Next Article in Journal
Intrauterine Transmission of Zika and Vertical Transfer of Neutralizing Antibodies Detected Immediately at Birth in Oaxaca, Mexico: An Analysis in the Context of Microcephaly
Previous Article in Journal
New Approaches to Tackling Intractable Issues in Infectious Disease
Previous Article in Special Issue
Bioleaching Mercury from Coal with Aspergillus flavus M-3
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Microorganisms
Volume 12
Issue 3
10.3390/microorganisms12030422
microorganisms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Roles and Regulation of Quorum Sensing of Acidophiles in Bioleaching: A Review

by
Wang Luo
1,2,
Yiran Li
1,2,
Shiqi Chen
1,2,
Yili Liang
1,2 and
Xueduan Liu
1,2,*
1
School of Minerals Processing and Bioengineering, Central South University, Changsha 410083, China
2
Key Laboratory of Biometallurgy, Ministry of Education, Changsha 410083, China
*
Author to whom correspondence should be addressed.
Microorganisms 2024, 12(3), 422; https://doi.org/10.3390/microorganisms12030422
Submission received: 10 January 2024 / Revised: 15 February 2024 / Accepted: 17 February 2024 / Published: 20 February 2024
(This article belongs to the Special Issue Microorganisms around Coal Mines and Their Application)
Browse Figure
Versions Notes

Abstract

:
Bioleaching has gained significant attention as a cost-effective and environmentally friendly approach for extracting metals from low-grade ores and industrial byproducts. The application of acidophiles in bioleaching has been extensively studied. Among the various mechanisms leaching microorganisms utilize, quorum sensing (QS) is pivotal in regulating their life activities in response to population density. QS has been confirmed to regulate bioleaching, including cell morphology, community structure, biofilm formation, and cell metabolism. Potential applications of QS have also been proposed, such as increasing mineral leaching rates by adding signaling molecules. This review is helpful for comprehensively understanding the role of QS in bioleaching and promoting the practical application of QS-based strategies in bioleaching process optimization.

1. Introduction

Bioleaching is a process that involves the use of microorganisms to extract valuable elements from ores [1]. This technology offers a range of benefits such as low cost, short processing time, environmental friendliness, and minimal pollution [2]. As a result, bioleaching has become a leading technology in the field of mineral processing around the world [3]. Many acidophilic microorganisms thrive in acid mine drainage, exhibiting remarkable adaptability, and can be applied to bioleaching and mitigating heavy metal contamination [1,4,5,6].
Microorganisms dissolve metals by non-contact or contact mechanisms [7,8]. Acidophilic microorganisms use inorganic sulfur compounds to produce sulfate while converting Fe2+ and Fe3+, playing important roles in global sulfur and iron cycling (Table 1) [9,10]. Over the last decade, there has been a gradual increase in the discussion surrounding leaching biofilms [11,12,13,14,15]. The attachment of cells to solid surfaces is an essential step in initiating bioleaching, as it forms the biofilm and is critical to the mineralization process [16]. Bacterial cells attached to surfaces produce extracellular polymers (EPS) associated with biofilm formation [17]. This process is thought to be mediated by quorum sensing (QS) [18].
QS is an important mechanism by which microorganisms regulate their life activities based on population density [26]. When the number of microorganisms in an area increases enough, they exhibit “social” behavior. These microorganisms use autoinducers (AIs) secreted into their environment to determine their population density. As the density of the bacterial population increases, the concentration of AIs also increases in the surrounding environment [27]. AIs are transported across the cell membrane, where they bind to corresponding receptors. This binding initiates a cascade of reactions regulating physiological and biochemical processes, such as root nodulation, bioluminescence, protein secretion, motility, virulence factor production, plasmid transfer, and biofilm formation [28,29,30].
According to different AIs, the QS pathways are divided into seven types. AI oligopeptides are found in Gram-positive bacteria [31]. The remaining six signaling pathways are distributed in Gram-negative bacteria: AHL (AI-1), AI-2, and CAI-1, first discovered in Vibrio [32,33], PQS signaling in Pseudomonas aeruginosa [34], AI-3 signaling in Escherichia coli O157:H7 [35], and DSF in Xanthomonas campestris [36]. QS commonly found in biofilm formation has also been observed in bioleaching systems [37]. In the early 21st century, Acidithiobacillus ferrooxidans was reported to have a functional N-acyl homoserine lactones (AHL) QS system by Farah et al. [38]. Rivas et al. discovered that A. ferrooxidans has another QS system, an atypical one consisting of glyQ, glyS, gph, and act genes [39]. Bellenberg et al. demonstrated an interspecies QS signaling mechanism for functional diffusion signaling factor (DSF) production by Leptospirillum ferriphilum and Leptospirillum ferrooxidans [40]. In addition to AHLs, acidophiles have enzyme systems encoding second messenger cyclic di-guanosine (c-di-GMP) that assist in regulating the QS system [41]. Huang et al. revealed the presence of AHL, autoinducer-3, DSF, and AHL-degrading enzymes by annotating the genome of 83 species of acidophiles [42]. Bioinformatics prediction and laboratory experiments have identified the QS system in acidophiles.
However, the role and function of QS in bioleaching systems have not been systematically summarized and discussed. Therefore, we searched the literature from the Web of Science database by using the keywords “bioleaching”, “acidophiles”, and “quorum sensing”, screened more than 120 documents that fit the topic, and reviewed the theoretical and practical understanding of QS in bioleaching. This paper provides a brief overview of the QS mechanisms in acidophiles, describing in detail the interconnections between the different mechanisms. Then, its role in cell morphology, community structure, biofilm formation, and microbial metabolism is summarized, emphasizing the exogenous regulation of QS on various bioleaching processes in acidophiles. The challenges and future development directions of QS-based control strategies are discussed. This information shows the great potential of QS in bioleaching regulation and contributes to the further development of QS-based control technologies.

2. QS and Second Messenger in Acidophiles

At present, the main QS systems studied in acidophiles are AHL and DSF systems, and c-di-GMP systems related to QS systems are also partially studied (Table 2). The same bacterium can contain multiple QS systems at the same time, and there are cascade, parallel, and competitive relationships between different systems. Different bacteria can communicate by generating, binding, and degrading the same AIs to adapt to extreme environments and improve competitiveness.

2.1. N-Acyl Homoserine Lactones System

The most extensively studied QS system in acidophiles is the AHL type. This system consists of at least four elements: AHLs, AHL synthase proteins, transcriptional regulators belonging to the family of R proteins, and cis-activated palindromic DNA sequences that serve as targets for R-AHL binary complexes [47]. As the density of bacteria increases, AHL gradually accumulates. As the population density attains a critical “quorum”, these AHL molecules surpass a threshold concentration, thereby banding with receptors known as R proteins, subsequently governing the transcription of target genes through their intricate interaction with multiple promoters or their detachment from their corresponding promoter regions [48]. A jump-start mechanism exists for quorum sensing, and when the signal is inhibited, for example by group interference, the pathway can still be activated [49].
Some acidophiles, such as A. ferrooxidans, possess a fully functional AfeI/R-type QS system, capable of synthesizing and responding to AIs. Two QS systems have been found in A. ferrooxidans. The first set (AHL-QS) is typical of the LuxI/R type, including the functional genes afeI, afeR, and the unknown functional gene orf3: afeI encodes an AHL synthase that synthesizes AHL. The gene afeR encodes an AHL receptor protein, which is the transcriptional regulator of the LuxR family of proteins [43]. It has been demonstrated that afeR exhibits a specific binding affinity towards the regulatory region of the afeI gene [50]. Moreover, afeI and afeR are preferentially expressed early in the stabilization phase [43]. The cis-regulatory components of afeR and orf3 coincide with the -35 promoter region, suggesting that AfeR may be capable of self-regulation [51]. The second set is an atypical QS system containing glyQ, glyS, gph, and act genes; the four genes are located in the same operon and encode aminoacetic acid tRNA synthetase, phosphorylase, and acyltransferase [39].
Other acidophiles also contain the AfeI homologous protein with the ability to synthesize AIs. The presence of an AHL-QS locus in L. ferrooxidans differs from the structural organization of A. ferrooxidans [45]. This locus consists of two convergent genes for the leptospiral lttR and lttI, and a third ORF has been found in the lttIR intergenic region [45]. A SdiA-like protein has been identified in Acidithiobacillus thiooxidans as strongly likely to take part in QS transcriptional regulation [44]. SdiA is an orphan QS transcriptional regulator, independent of the AHL synthase. Orphan QS transcriptional regulators can perceive AHLs from other bacteria in microbial consortia and are key molecules for QS flexibility and adaptation [52].
An acidophilic bacterium can produce multiple variants of AHL. The transport of the same AHL into the extracellular environment can cause the recognition of a variety of bacteria. A. ferrooxidans and A. thioooxidans produce AHL [45]. S-adenosyl-L-methionine is acylated by AHL synthase and reacts with an acyl–acyl carrier protein (acyl-ACP) to produce AHL [53] (Figure 1). Under different culture conditions, a single bacterium can produce 24 different kinds of AHLs [54]. A. ferrooxidans synthesizes AHLs with acyl chains ranging from 8 to 16 carbon atoms in length, which exhibit oxygen and hydroxyl substitutions at the third carbon position [55]. The preference for unsubstituted, 3-oxo, or 3-hydroxy acyl-ACP substrates is believed to stem from the inherent selectivity of the AHL synthase towards specific subgroups of acyl-ACP compounds generated through the reductive condensation cycle of fatty acid biosynthesis [56]. A. thioooxidans produces C10- and C12-HSL [17]. C12- and C14-HSL synthesized by A. ferrooxidans show detectable increases in the early stabilization period [43].

2.2. Diffusible Signal Factor System

DSF-mediated intraspecific communication pathways belong to different taxa [57]. In Xcc, DSF ((Z)-11-methyl-2-dodecenoic Acid) synthesis relies on adjacent rpfF and rpfB genes in the rpf gene cluster, which encode the putative enoyl-CoA hydrase and the putative long-chain fatty acid acyl-CoA ligase [58]. Bacteria produce DSF through the bifunctional enzyme RpfF and the classical fatty acid synthesis pathway, and RpfC controls synthesis through its receiver domain to form a complex with RpfF [59]. After a QS response, the system can be induced to restore DSF levels to pre-QS levels [60].
Genes encoding DSF family signaling-specific two-component systems or response regulators and genes suitable for DSF signaling sensing have been discerned within the genomes of Acidithiobacillus caldus, L. ferriphilum, L. ferrooxidans, and Sulfobacillus thermosulfidooxidans [40,61]. The L. ferriphilum DSM 14647T genome contains a gene cluster containing the DSF system, which consists of the gene rpfF encoding a diffusion signaling factor synthase, genes encoding rpfC homologs, and their respective two-component systems of response modifier genes rpfG [62]. The biosynthesis of the diffusible signal factor in Leptospirillum spp. represents a sophisticated ecological niche defense mechanism aimed at safeguarding its habitat and countering antagonistic microorganisms.

2.3. Cyclic Dimeric Guanosine Monophosphate System

The c-di-GMP pathway proves to be the most versatile second messenger in acidophiles [63]. The regulation of c-di-GMP concentration relies on the antagonistic actions of di-guanosine cyclases (DGCs) and phosphodiesterases (PDEs) [63]. This pathway converts both environmental conditions and intracellular signals into different concentrations of c-di-GMP, which regulates flagellar motility, substrate attachment, and biofilm development by binding to different effector proteins, such as the PilZ domain, FleQ, and PelD proteins [63].
A. ferrooxidans, A. thiooxidans, and A. caldus have functional c-di-GMP pathways [46,64]. Several putative ORFs encoding DGC, PDE, and effector proteins have been identified in the study of Acidithiobacillus species. Cyclic-di-GMP is synthesized by DGCs, whereas PDEs catalyze the degradation of c-di-GMP to 5′-phosphoguanylyl-(3′-5′)-guanosine (pGpG) and GMP [65,66]. DGC activity resides in the GGDEF domain, while PDE activity resides in two unrelated domains: EAL and HD-GYP [63]. Two c-di-GMP effector proteins with PilZ domains have been identified in the genome of A. ferrooxidans, which showcases their pivotal role in controlling biofilm formation and mineral colonization [41]. The bcs operon encoding cellulose synthesis is widely found in acidophiles, while the PEL operon encoding PEL extracellular polysaccharide synthesis is only found in A. caldus and A. thiooxidans [44]. They are involved in biofilm formation in the Acidithiobacillus species [41,67].

3. Interactions between Different Systems

The AHL-QS system and the DSF system interact with each other in acidophiles. The AHL-QS-related genes and the DSF system are present in L. ferriphilum, where genes encoding the DSF system are expressed at high levels, whereas RNA transcripts of the genes encoding orphan LuxR proteins are very low [62]. The number of rpfF transcripts increases after AHL addition to L. ferriphilum [40]. The level of flrB (influencing bacterial adhesion, motility, biofilm formation, and EPS production) transcripts is reduced in L. ferriphilum after treatments involving DSF/BDSF and AHLs [40]. AHL-QS affects the expression of DSF synthesis genes and regulates the transcription of downstream genes such as flrB. Whether there is a specific cascade, cooperation, and competition relationship between the AHL system and the DSF system remains to be explored.
QS can either promote or inhibit biofilm growth, depending on the existence or nonexistence of environmental cues that influence c-di-GMP signaling [68]. The GGDEF/EAL domain is preferentially expressed in the biofilm state of Leptospirillum spp. living with A. ferrooxidans [41]. An unknown AHL receptor binding 3-oxo-C8-HSL (N-(3-Oxooctanoyl)-L-homoserine lactone) can directly promote pel manipulator expression and facilitate the biosynthesis of PEL exopolysaccharides of A. thiooxidans [44]. QS systems and c-di-GMP pathway connections, under the influence of environmental signals and cell density, transform A. ferrooxidans from a planktonic to biofilm lifestyle [41].
The DSF system is associated with c-di-GMP degradation and synthesis. RpfG contains typical receptor structural, and HD-GYP structural, domains, and RpfG controls the expression of a panel of proteins with GGDEF or EAL domains that may be involved in the synthesis or degradation of c-di-GMP [66,69]. It has been found that the DSF system can activate the HD-GYP of the RpfG domain and enzymatically regulate c-di-GMP metabolism, bacterial signaling, and response to environmental signals [70,71].

4. The Role of QS in Bioleaching

QS has been extensively studied and proven to affect various aspects of cell morphology, community structure, biofilm formation, and cell metabolism in regulating the bioleaching process.

4.1. Cell Morphology

Flagellar gene clusters are distributed in almost all Acidithiobacillus species except A. ferrooxidan and Acidithiobacillus ferridurans, where sulfur oxidizers containing the Sox system tend to form flagella [72,73]. Certain acidophiles that have been isolated have flagella to enhance attachment to minerals [74,75]. A series of genes related to flagellar synthesis, such as flgA~K and fliC, have been identified in the downstream genes of the QS system of the strain, which can regulate bacterial motility and chemotaxis [76]. QS exerts an indisputable influence on the intricate process of flagella formation, subsequently impacting cellular locomotion and chemotaxis.

4.2. Community Structure

Secretion and response systems for AIs are universally distributed in bacterial communities [77]. Microorganisms perceive AIs and subsequently alter their behavior, consequently exerting influences on the collaborative and antagonistic dynamics among microorganisms, thereby engendering modifications within the intricate web of microbial assemblages [78].
QS affects bacterial community composition through a combination of mechanisms [79]. QS can regulate the production of “public goods” that provide public compounds or functions such as extracellular hydrolases or siderophores [80,81,82]. The coordination of enzyme production through QS ensures an optimal distribution of resources and energy utilization within the microbial community, maximizing the efficiency of metal extraction. In addition, QS regulatory mechanisms can affect microbial communities through the production of antimicrobial compounds [83,84]. Changes in bacterial community composition driven by QS may be due to the chemical properties of AIs themselves, including their antimicrobial activity and iron-chelating properties [85,86]. Unsaturated fatty acids have been identified as compounds possessing antimicrobial properties that function by perturbing the cellular membranes of Gram-positive bacteria [87]. Simultaneously, DSF also falls within this classification of lipids. The recognition and reaction of L. ferriphilum bacteria to DSF encompasses not only the regulation of the QS signal but also the acid stress response to uptake the DSF molecule itself.

4.3. Biofilm Formation

Biofilms exist as a protective barrier for microorganisms during bioleaching. By coordinating the attachment and detachment of cells, QS enables microbial communities to collectively attach to mineral surfaces, forming biofilms that can protect microorganisms from extreme environmental conditions [88,89]. Zhang et al. proposed a model for the biofilm formation of bacterial strains in bioleaching [90,91,92]: Firstly, the cells reversibly attach to the mineral surface while producing adherent EPS compounds [93,94]. Secondly, the cells are firmly attached to the pyrite surface and colonize it; small microcolonies can also be interconnected by EPS or cellular appendages [90,95]. Finally, large colonies and erosion pits form as the cell surface erodes. The cells are encapsulated in an EPS layer dominated by carbohydrates and proteins [90,96]. The different stages of biofilm formation in acidophiles are regulated by the QS system (Figure 1).
The regulation of biofilm formation encompasses bacteria movement, EPS production, intracellular signaling, and intercellular communication [97]. The QS network accounts for at least 4.5% of the A. ferrooxidans ATCC 23270T genome, of which 42.5% are associated with biofilm formation [50]. The identification of genes in the synthesis of EPS conveys that the QS pathway of A. ferrooxidans could potentially be linked to biofilm formation [98]. The c-di-GMP pathway is likewise important in biofilm formation. The high levels of c-di-GMP in adhesive cells, as compared to planktonic cells, suggest the involvement of the c-di-GMP pathway in biofilm formation in A. ferrooxidans [41]. A similar phenomenon has been observed in A. thiooxidans as well [64]. In addition, DGCs of A. thiooxidans couple the GGDEF structural domain to n-terminal signaling structural domains involved in signaling perception at the extracellular, membrane, and extraplasmic levels [99]. This strongly suggests that A. caldus regulates group movement and adhesion to sulfur surfaces through the c-di-GMP pathway [100]. A. thiooxidans and A. caldus have multiple copies of the fleQ gene, and 3-oxo-C8 -HSL may promote transcription of the gene encoding fleQ, thereby inducing biosynthesis of PEL exopolysaccharides [44]. PeL-like polysaccharides give active play in A. thiooxidans attachment to solid energy substrates [64]. The L. ferriphilum genome has identified genes encoding the PilZ domain that are functionally associated with the biosynthesis and export of cellulose and EPS, suggesting that c-di-GMP metabolism drives L. ferriphilum EPS production [40]. The expression of the effector proteins PelD and PilZ promotes the formation of acidophilic biofilms [67].

4.4. Microbial Metabolism

QS is intricately linked to the metabolic processes of bacteria, whereby the expression of genes induced by AHLs governs the synthesis and breakdown of metabolites. Ranava et al. postulated that QS is a protected function that operates independently from direct metabolic pathways [101]. On the other hand, DSF facilitates the reinforcement of the metabolic system, bolstering defense against infiltration, facilitating Na+ extrusion, aiding in iron absorption, and clearing reactive oxygen species [102]. The influence of AI-2 on metabolism is equally noteworthy, as it notably enhances fatty acid elongation, amino acid metabolism, and phosphorus relay signaling [103]. In bioleaching, QS acts as a harmonizing conductor, facilitating the synchronization of various metabolic processes vital to the successful extraction of metals from ores.
The sulfur and iron metabolism of acidophiles is closely related to their rapid adaptation to nutrient deprivation and extreme survival environments. A. ferrooxidans has two different AHL-based QS mechanisms, one based on Act and the other on the AfeI/R QS system. The expression of the gene act is more up-regulated in an iron-containing medium than in a sulfur-containing medium. At the same time, the reverse is true for the AfeI/R QS system, which is more up-regulated in a sulfur-containing medium than in an iron-containing medium, suggesting that these signals are related to the ability of A. ferrooxidans to colonize and utilize different sulfur- and iron-containing minerals [39]. Differences in energy substrates may be responsible for the changes in AHLs. A. ferrooxidans synthesizes acyl HSLs with C-3 hydrogen and hydroxyl substituents in a sulfur-rich medium, whereas only 3-OH-HSLs are found in an Fe2+ -rich medium [104]. 3-OH-C14-HSL(N-(3-Hydroxytetradecanoyl)-DL-homoserine lactone) works when A. ferrooxidans is cultivated with sulfur, but has no effect on growth when A. ferrooxidans is cultivated with Fe2+. The QS system regulates the microbial ability to utilize, assimilate, and sequester iron by modulating the secretion of specific EPS components, Fe3+-reductase, siderophores, and other relevant iron uptake factors [105]. The substrate-based regulatory model of acidophiles may be an important mechanism for them to gain a competitive advantage in extreme environments.

5. Regulation of QS in Bioleaching

QS modulation is a phenomenon influenced by the concentration of molecules. The current modulation techniques aim to augment the abundance of AIs within bioleaching through direct or indirect mechanisms. According to the different sources of AIs, the existing QS-based regulatory methods can be divided into endogenous regulation and exogenous regulation.

5.1. Endogenous Regulation

At present, endogenous QS-based regulation in bioleaching is mainly achieved by constructing engineered strains. AHL-QS-overexpressing strains show significant differences in biofilm formation. The cultivation of A. ferrooxidans in pyrite and the overexpression of AHL-QS led to a significant increase in EPS synthesis [106]. Overexpression of the AHL-QS or the afeI-only gene strains shows enhanced adhesion to cobaltite [107]. Overexpression of afeI stimulates the synthesis of EPS, further enhancing cellular adhesion to and bioerosion of sulfur [104]. The cell growth and sulfur metabolism of the overexpression of the afeI strain are significantly higher than the control strain during the logarithmic growth phase when in a sulfur-containing medium [104]. The gene afel overexpression promotes the sulfur metabolism of cells in the pre- and mid-culture period, and genes involved in periplasmic and cytoplasmic sulfation, including the hdr operon, doxDA operon, and cyo genes, are up-regulated [104]. The concentration of AHLs is key to determining whether afeI plays a regulatory role. In a sulfur-containing medium, when the concentration of AHLs reaches a threshold, the AfeI/R system is activated, accelerating cell growth. However, the regulation of A. ferrooxidans by AfeI/R can be considered a potent “inhibitor” of cell growth and cell density when cultured with an iron-containing medium. Overexpression of afeI inhibits ferrous oxidation and the cell growth of A. ferrooxidans [104]. Genes involved in ferrous oxidation and electron transport, including rus operon and pet operon, are significantly down-regulated in afel overexpression strains [104]. Transcriptomic analysis has revealed the up-regulation or down-regulation of gene expression by AHLs, but the regulatory mechanisms of QS in acidophiles still need further exploration.

5.2. Exogenous Regulation

Compared with endogenous regulation, exogenous regulation can directly increase the concentration of AIs in biological leaching, thereby more directly activating QS regulation. AHL is the most widely studied class of AIs in exogenous regulation. Exogenous AIs play an important role in regulating bioleaching (Table 3).

5.2.1. N-Acyl Homoserine Lactones

The difference in community composition has a significant effect on the leaching rate. Exogenous AHL leads to changes in the structure of bacterial communities, not only in AHL-mediated QS bacteria but also in other microorganisms that use auto-inducible peptides for communication [110,111,112]. Exogenous C14-HSL increases the adhesion of native A. ferrooxidans cells to pyrite in a mixed bioleaching community [98]. Exogenous AHLs modulate the microbial community structure to increase the final ratio of functional strains and facilitate the hydrolysis of difficult-to-biodegrade organics [110,113,114].
Early adsorption of cells is the key to biofilm formation [115]. The addition of AHL affects cell attachment by different species of acidophiles [17]. QS increases the attachment of A. ferrooxidans to pyrite and sulfur by the addition of the AHL molecule [98]. The AHL mixture inhibits A. ferrooxidans ATCC 23270 attachment to pyrite with a small but significant trend [55]. Similar research indicates that an AHL mixture consisting of hydroxy-AHL and oxo-AHL inhibits both the rate and degree of bacterial adhesion to pyrite [45].
EPS mainly comprises proteins, polysaccharides, fatty acids, and metal ions, and multiple components promote mineral leaching [116,117,118,119,120]. EPS interacts with iron-containing minerals through the formation of P-O-Fe bonds, thereby inducing microbial adhesion and EPS accumulation [97]. AHL molecules with long acyl chains promote EPS formation, as well as increasing A. ferrooxidans attachment on sulfur and pyrite surfaces [98,104]. Adding C8-, 3-oxo-C8-, or C10-AHL enhances A. thiooxidans biofilm formation on sulfur substrates [17]. AHL selectively promotes the synthesis of amino acids and promotes extracellular protein content [121]. AHL facilitates the synthesis of acidophile EPS and augments its resilience in arduous environments.
The addition of AHL affects iron–sulfur metabolism and bioleaching. The addition of an AHL mixture inhibits the biofilm formation of Acidithiobacillus ferrivorans SS3, Acidiferrobacter sp. SPIII/3, and L. ferrooxidans DSM 2391, with a decrease in pyrite leaching [108]. The carbon felt electrodes in the biobattery are pre-colonized by A. ferrooxidans ATCC 23270 by the addition of C14-AHLs and with Fe2+ as an electron donor, and their current output, from −0.31 A m−2, increases to −0.56 A m−2, suggesting that C14-HSL has a significant impact on A. ferrooxidans ATCC 23270 [122]. Exogenous AHLs enhance the ability of Acidithiobacillus and Pseudomonas to extract metals from discarded printed circuit boards [123]. An in-depth understanding of the mechanism of AHL-QS regulation of iron–sulfur metabolism in acidophiles could be a useful tool for the development of bioleaching [124]. Acidophiles may utilize the QS system to establish a co-evolutionary process that regulates responses from energy substrates to cell growth and population density, which is an important pathway for chemotrophic autotrophs to adapt to growth environments and gain ecological competitive advantages.

5.2.2. N-Acyl Homoserine Lactones Analogues

Different AHL analogues promote or inhibit the attachment of acidophiles and the formation of EPS. The AHL analogue 4-phenyl-3-yloxy-HSL derivative decreases attachment levels upon addition, while some AHL analogues, such as 3-sulfonylamide-C8-HSL, induce an increase in attachment levels [45]. Tetrazole accelerates the adsorption of A. ferrooxidans to sulfur flakes and up-regulated afeI and zwf (involved in the intracellular levels of α-D-glucose-6 phosphate) gene expression [109]. Tetrazole 9c triggers the QS system by inducing gene expression that allows AHL efflux [50]. Meanwhile, tetrazole 9c inhibits several genes involved in carbohydrate metabolism, directing carbon flow to the synthesis of maltodextrin to increase adhesion, accumulating α-D-glucose-6 phosphate and α-D-glucose-1-phosphate associated with EPS precursor biosynthesis to promote biofilm formation [50].

5.2.3. Diffusible Signal Factor

Exogenous DSF affects the leaching efficiency of acidophiles in bacterial attachment and iron–sulfur oxidation. Mineral-attached A. caldus, L. ferriphilum, and S. thermosulfidooxidans on mineral particles are reduced by the addition of DSF [61]. The reduced attachment rate to chalcopyrite may contribute to the reduced oxidation of Fe2+ [40]. The addition of DSF inhibits the oxidation of the soluble substrate Fe2+ or the insoluble substrate chalcopyrite in L. ferriphilum, S. thermosulfidooxidans, and A. ferrooxidans [61].
DSF mediates interspecific interactions. L. ferriphilum is dominant in the community after DSF addition [61]. DSF inhibits Fe2+ oxidation in post-inoculated S. thermosuldooxidans, contributing to a preference for the oxidation of inorganic sulfur compounds by S. thermosuldooxidans when co-cultured with L. ferriphilum [40]. L. ferrooxidans DSM 2391 and Acidiferrobacter sp. SPIII/3 inhibit each other during leaching, and the inhibition between the strains can be partially overcome by the addition of a mixture of C8-, C14-, and C1618-HSL, which increases the pyrite leaching rate [108]. One of the reasons may be due to the high sensitivity of Acidiferrobacter sp. SPIII/3 to DSF/BDSF secreted by L. ferrooxidans to inhibit growth or even lead to cell lysis, whereas AHL may inhibit L. ferrooxidans [40]. The addition of DSF and AHL reduces the number of transcript counts of L. ferriphilum flagellar-related genes [40]. AHL and DSF synergistically regulate the adaptation of acidophiles to extreme environments and mineral leaching.

6. Research Needs and Future Direction

While previous studies have shown that QS-based bioleaching control methods are useful at laboratory scales, more needs to be done at the pilot and industrial scales. The existing endogenous and exogenous regulatory methods need to be optimized. In addition, it is necessary to understand the regulatory mechanism of QS in bioleaching for future technology development. While previous research has provided insights into the molecular mechanism and impact of QS on individual strains, there is a lack of literature on the intricate signaling communication among different species of bacterial communities. Additionally, a comprehensive investigation into strain-to-strain communication within the same QS system is warranted. Previous studies have primarily focused on the AHL and DSF systems as AIs systems, leaving room for further experimental evidence to confirm the existence of additional QS systems in acidophiles. Moreover, there is great value in exploring the communication and interconnectedness between different QS systems. Acidophiles still require a thorough understanding of their secretion of AIs and the interaction of genes related to iron–sulfur oxidation. To better understand the above mechanisms, it is necessary to synthesize microbial communities and study the response behavior of QS in mixed microbial systems. Finally, a model of the relationship between different types of QS systems and passivation film formation and biofilm development in bioleaching should be established, so that the whole bioleaching system affected by QS can be directly evaluated with specific indicators. The study of the QS system of acidophiles has helped to unravel the underlying mechanisms that control biofilm formation in bioleaching. Additionally, delving deeper into the underlying mechanisms of QS in bioleaching could potentially lead to the discovery of novel microbial species with enhanced metal solubilization capabilities. Furthermore, comprehending the QS system in acidophilics also advances our knowledge of other functional microorganisms.

7. Conclusions

In previous studies, the mechanism of the QS system in acidophiles and its role in biological leaching has been explored by constructing overexpression strains and adding exogenous AIs. However, the research is limited to the laboratory scale, and future research needs to develop to medium and large scales, such as column leaching and heap leaching. Moreover, the strains and QS systems studied are relatively limited; it is necessary to expand the scope of research, construct a coupling model of the QS system and bioleaching system in the microbial community, and explore a reproducible, easy-to-operate and low-cost method to improve bioleaching efficiency.

Author Contributions

Conceptualization, W.L. and Y.L. (Yili Liang); resources, W.L. and Y.L. (Yiran Li); writing—original draft preparation, W.L.; writing—review and editing, W.L., Y.L. (Yiran Li) and S.C.; visualization, W.L.; supervision, Y.L. (Yili Liang) and X.L.; project administration, Y.L. (Yili Liang) and X.L.; funding acquisition, Y.L. (Yili Liang) and X.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the following grants: National Natural Science Foundation of China (52174341) and Graduate Research and Innovation Project (1053320220937) at Central South University, China.

Data Availability Statement

No new data were created or analyzed in this study. Data sharing is not applicable to this article.

Acknowledgments

All the Figures in Table 2 were drawn by Kingdraw. Figure 1 in the manuscript was drawn by Figdraw.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

AbbreviationFull Name
QSquorum sensing
EPSextracellular polymers
AIsautoinducers
AHLN-acyl homoserine lactones
c-di-GMPcyclic di-guanosine
DGCsdiguanylate cyclases
PDEsphosphodiesterases
pGpG5′-phosphoguanylyl-(3′-5′)-guanosine
DSFdiffusible signal factor
BDSFBurkholderia diffusible signal factor
AHL-QSAfeI/R-type QS system
SAMS-adenosyl-L-methionine
acyl-ACPacyl–acyl carrier protein
HSL homoserine lactone
OH-HSLhydroxy-homoserine lactone
oxo-HSLoxygen-homoserine lactone
3-oxo-C8-HSLN-(3-Oxooctanoyl)-L-homoserine lactone
3-OH-C14-HSLN-(3-Hydroxytetradecanoyl)-DL-homoserine lactone

References

  1. Wang, X.; Ma, L.; Wu, J.; Xiao, Y.; Tao, J.; Liu, X.D. Effective bioleaching of low-grade copper ores: Insights from microbial cross experiments. Bioresour. Technol. 2020, 308, 123273. [Google Scholar] [CrossRef]
  2. Gu, T.; Rastegar, S.O.; Mousavi, S.M.; Li, M.; Zhou, M. Advances in bioleaching for recovery of metals and bioremediation of fuel ash and sewage sludge. Bioresour. Technol. 2018, 261, 428–440. [Google Scholar] [CrossRef]
  3. Roberto, F.F.; Schippers, A. Progress in bioleaching: Part B, applications of microbial processes by the minerals industries. Appl. Microbiol. Biotechnol. 2022, 106, 5913–5928. [Google Scholar] [CrossRef]
  4. Zhang, R.; Bellenberg, S.; Neu, T.; Sand, W.; Vera, M. The biofilm lifestyle of acidophilic metal/sulfur-oxidizing microorganisms. In Biotechnology of Extremophiles: Grand Challenges in Biology and Biotechnology; Rampelotto, P., Ed.; Springer: Cham, Switzerland, 2016; pp. 177–213. [Google Scholar]
  5. Li, L.; Liu, Z.; Zhang, M.; Meng, D.; Liu, X.; Wang, P.; Li, X.; Jiang, Z.; Zhong, S.; Jiang, C.; et al. Insights into the metabolism and evolution of the genus Acidiphilium, a typical acidophile in acid mine drainage. mSystems 2020, 5, e00867-20. [Google Scholar] [CrossRef]
  6. Zhang, X.; Liu, X.; Liang, Y.; Xiao, Y.; Ma, L.; Guo, X.; Miao, B.; Liu, H.; Peng, D.; Huang, W.; et al. Comparative genomics unravels the functional roles of co-occurring acidophilic bacteria in bioleaching heaps. Front. Microbiol. 2017, 8, 790. [Google Scholar] [CrossRef]
  7. Rawlings, D.E. Heavy metal mining using microbes. Annu. Rev. Microbiol. 2002, 56, 65–91. [Google Scholar] [CrossRef]
  8. Sand, W.; Gehrke, T.; Jozsa, P.; Schippers, A. (Bio)chemistry of bacterial leaching—Direct vs. indirect bioleaching. Hydrometallurgy 2001, 59, 159–175. [Google Scholar] [CrossRef]
  9. Quatrini, R.; Johnson, D.B. Microbiomes in extremely acidic environments: Functionalities and interactions that allow survival and growth of prokaryotes at low pH. Curr. Opin. Microbiol. 2018, 43, 139–147. [Google Scholar] [CrossRef]
  10. Ma, L.; Huang, S.; Wu, P.; Xiong, J.; Wang, H.; Liao, H.; Liu, X. The interaction of acidophiles driving community functional responses to the re-inoculated chalcopyrite bioleaching process. Sci. Total Environ. 2021, 798, 149186. [Google Scholar] [CrossRef]
  11. Vardanyan, A.; Vardanyan, N.; Khachatryan, A.; Zhang, R.; Sand, W. Adhesion to mineral surfaces by cells of Leptospirillum, Acidithiobacillus and Sulfobacillus from Armenian sulfide ores. Minerals 2019, 9, 69. [Google Scholar] [CrossRef]
  12. Moreno-Paz, M.; Gómez, M.J.; Arcas, A.; Parro, V. Environmental transcriptome analysis reveals physiological differences between biofilm and planktonic modes of life of the iron oxidizing bacteria Leptospirillum spp. in their natural microbial community. BMC Genom. 2010, 11, 404. [Google Scholar] [CrossRef]
  13. Ye, M.; Liang, J.; Liao, X.; Li, L.; Feng, X.; Qian, W.; Zhou, S.; Sun, S. Bioleaching for detoxification of waste flotation tailings: Relationship between EPS substances and bioleaching behavior. J. Environ. Manag. 2020, 279, 111795. [Google Scholar] [CrossRef] [PubMed]
  14. Li, Q.; Sand, W. Mechanical and chemical studies on EPS from Sulfobacillus thermosulfidooxidans: From planktonic to biofilm cells. Colloids Surf. B 2017, 153, 34–40. [Google Scholar] [CrossRef] [PubMed]
  15. Li, Z.; Wang, X.; Wang, J.; Yuan, X.; Jiang, X.; Wang, Y.; Zhong, C.; Xu, D.; Gu, T.; Wang, F. Bacterial biofilms as platforms engineered for diverse applications. Biotechnol. Adv. 2022, 57, 107932. [Google Scholar] [CrossRef] [PubMed]
  16. Rohwerder, T.; Gehrke, T.; Kinzler, K.; Sand, W. Bioleaching review part A: Progress in bioleaching: Fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl. Microbiol. Biotechnol. 2003, 63, 239–248. [Google Scholar] [CrossRef] [PubMed]
  17. Bellenberg, S.; Díaz, M.; Noël, N.; Sand, W.; Poetsch, A.; Guiliani, N.; Vera, M. Biofilm formation, communication and interactions of leaching bacteria during colonization of pyrite and sulfur surfaces. Res. Microbiol. 2014, 165, 773–781. [Google Scholar] [CrossRef]
  18. Whiteley, M.; Diggle, S.P.; Greenberg, E.P. Progress in and promise of bacterial quorum sensing research. Nature 2017, 551, 313–320. [Google Scholar] [CrossRef] [PubMed]
  19. Zhang, X.; Liu, X.; Liang, Y.; Fan, F.; Zhang, X.; Yin, H. Metabolic diversity and adaptive mechanisms of iron- and/or sulfur-oxidizing autotrophic acidophiles in extremely acidic environments. Environ. Microbiol. Rep. 2016, 8, 738–751. [Google Scholar] [CrossRef] [PubMed]
  20. Chen, L.-X.; Huang, L.-N.; Méndez-García, C.; Kuang, J.; Hua, Z.; Liu, J.; Shu, W. Microbial communities, processes and functions in acid mine drainage ecosystems. Curr. Opin. Biotechnol. 2016, 38, 150–158. [Google Scholar] [CrossRef]
  21. Amouric, A.; Brochier-Armanet, C.; Johnson, D.B.; Bonnefoy, V.; Hallberg, K.B. Phylogenetic and genetic variation among Fe(II)-oxidizing acidithiobacilli supports the view that these comprise multiple species with different ferrous iron oxidation pathways. Microbiology 2011, 157, 111–122. [Google Scholar] [CrossRef]
  22. Weiner, J.H.; Ullrich, S.R.; Poehlein, A.; Tischler, J.S.; González, C.; Ossandon, F.J.; Daniel, R.; Holmes, D.S.; Schlömann, M.; Mühling, M. Genome analysis of the biotechnologically relevant acidophilic iron oxidising strain JA12 indicates phylogenetic and metabolic diversity within the novel genus “Ferrovum”. PLoS ONE 2016, 11, e0146832. [Google Scholar] [CrossRef]
  23. Méndez-García, C.; Mesa, V.; Sprenger, R.; Richter, M.; Diez, M.; Solano, J.; Bargiela, R.; Golyshina, O.; Manteca, Á.; Ramos, J.; et al. Microbial stratification in low pH oxic and suboxic macroscopic growths along an acid mine drainage. ISME J. 2014, 8, 1259–1274. [Google Scholar] [CrossRef] [PubMed]
  24. Urbieta, M.S.; Rascovan, N.; Vázquez, M.P.; Donati, E. Genome analysis of the thermoacidophilic archaeon Acidianus copahuensis focusing on the metabolisms associated to biomining activities. BMC Genom. 2017, 18, 445. [Google Scholar] [CrossRef] [PubMed]
  25. Dai, X.; Wang, H.; Zhang, Z.; Li, K.; Zhang, X.; Mora-López, M.; Jiang, C.; Liu, C.; Wang, L.; Zhu, Y.; et al. Genome sequencing of sulfolobus sp. A20 from Costa Rica and comparative analyses of the putative pathways of carbon, nitrogen, and sulfur metabolism in Various Sulfolobus Strains. Front. Microbiol. 2016, 7, 1902. [Google Scholar] [CrossRef] [PubMed]
  26. Williams, P.; Winzer, K.; Chan, W.C.; Camara, M. Look who’s talking: Communication and quorum sensing in the bacterial world. Philos. Trans. R. Soc. B 2007, 362, 1119–1134. [Google Scholar] [CrossRef]
  27. Sharma, A.; Singh, P.; Sarmah, B.K.; Nandi, S.P. Quorum sensing: Its role in microbial social networking. Res. Microbiol. 2020, 171, 159–164. [Google Scholar] [CrossRef] [PubMed]
  28. Fuqua, C.; Greenberg, E.P. Listening in on bacteria: Acyl-homoserine lactone signalling. Nat. Rev. Mol. Cell Biol. 2002, 3, 685–695. [Google Scholar] [CrossRef] [PubMed]
  29. Bassler, B.L.; Losick, R. Bacterially speaking. Cell 2006, 125, 237–246. [Google Scholar] [CrossRef]
  30. Williams, P. Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 2007, 153, 3923–3938. [Google Scholar] [CrossRef] [PubMed]
  31. Wu, S.; Liu, J.; Liu, C.; Yang, A.; Qiao, J. Quorum sensing for population-level control of bacteria and potential therapeutic applications. Cell. Mol. Life Sci. 2020, 77, 1319–1343. [Google Scholar] [CrossRef]
  32. Kuo, A.; Blough, N.V.; Dunlap, P.V. Multiple N-acyl-L-homoserine lactone autoinducers of Luminescence in the marine symbiotic bacterium Vibrio fischerit. J. Bacteriol. 1994, 176, 7558–7565. [Google Scholar] [CrossRef]
  33. Higgins, D.A.; Pomianek, M.E.; Kraml, C.M.; Taylor, R.K.; Semmelhack, M.F.; Bassler, B.L. The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 2007, 450, 883–886. [Google Scholar] [CrossRef]
  34. Pesci, E.C.; Milbank, J.B.; Pearson, J.P.; McKnight, S.; Kende, A.S.; Greenberg, E.P.; Iglewski, B.H. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 1999, 96, 11229–11234. [Google Scholar] [CrossRef]
  35. Sperandio, V.; Torres, A.G.; Jarvis, B.; Nataro, J.P.; Kaper, J.B. Bacteria–host communication: The language of hormones. Proc. Natl. Acad. Sci. USA 2003, 100, 8951–8956. [Google Scholar] [CrossRef] [PubMed]
  36. Barber, C.E.; Tang, J.L.; Feng, J.X.; Pan, M.Q.; Wilson, T.J.G.; Slater, H.; Dow, J.M.; Williams, P.; Daniels, M.J. A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol. Microbiol. 2003, 24, 555–566. [Google Scholar] [CrossRef] [PubMed]
  37. Vera, M.; Schippers, A.; Hedrich, S.; Sand, W. Progress in bioleaching: Fundamentals and mechanisms of microbial metal sulfide oxidation—Part A. Appl. Microbiol. Biotechnol. 2022, 106, 6933–6952. [Google Scholar] [CrossRef] [PubMed]
  38. Farah, C.; Vera, M.; Morin, D.; Haras, D.; Jerez, C.; Guiliani, N. Evidence for a functional quorum-sensing type AI-1 system in the extremophilic bacterium Acidithiobacillus ferrooxidans. Appl. Environ. Microbiol. 2005, 71, 7033–7040. [Google Scholar] [CrossRef] [PubMed]
  39. Rivas, M.; Seeger, M.; Jedlicki, E.; Holmes, D. Second acyl homoserine lactone production system in the extreme acidophile Acidithiobacillus ferrooxidans. Appl. Environ. Microbiol. 2007, 73, 3225–3231. [Google Scholar] [CrossRef]
  40. Bellenberg, S.; Salas, B.; Ganji, S.; Jorquera-Román, C.; Valenzuela, M.; Buetti-Dinh, A.; Unelius, C.R.; Dopson, M.; Vera, M. Diffusible signal factor signaling controls bioleaching activity and niche protection in the acidophilic, mineral-oxidizing leptospirilli. Sci. Rep. 2021, 11, 16275. [Google Scholar] [CrossRef] [PubMed]
  41. Ruiz, L.; Castro, M.; Barriga, A.; Jerez, C.; Guiliani, N. The extremophile Acidithiobacillus ferrooxidans possesses a c-di-GMP signalling pathway that could play a significant role during bioleaching of minerals. Lett. Appl. Microbiol. 2012, 54, 133–139. [Google Scholar] [CrossRef] [PubMed]
  42. Huang, S.; Liu, X.; Yang, W.; Ma, L.; Li, H.; Liu, R.; Qiu, J.; Li, Y. Insights into adaptive mechanisms of extreme acidophiles based on quorum sensing/quenching-related proteins. mSystems 2022, 7, e0149121. [Google Scholar] [CrossRef] [PubMed]
  43. Rivas, M.; Seeger, M.; Holmes, D.; Jedlicki, E. A Lux-like quorum sensing system in the extreme acidophile Acidithiobacillus ferrooxidans. Biol. Res. 2005, 38, 283–297. [Google Scholar] [CrossRef] [PubMed]
  44. Díaz, M.; Martin, D.S.; Castro, M.; Vera, M.; Guiliani, N. Quorum sensing signaling molecules positively regulate c-di-GMP effector PelD encoding gene and PEL exopolysaccharide biosynthesis in extremophile bacterium Acidithiobacillus thiooxidans. Genes 2021, 12, 69. [Google Scholar] [CrossRef] [PubMed]
  45. Ruiz, L.; Valenzuela, S.; Castro, M.; Gonzalez, A.R.; Frezza, M.; Soulère, L.; Rohwerder, T.; Queneau, Y.; Doutheau, A.; Sand, W.; et al. AHL communication is a widespread phenomenon in biomining bacteria and seems to be involved in mineral-adhesion efficiency. Hydrometallurgy 2008, 94, 133–137. [Google Scholar] [CrossRef]
  46. Castro, M.; Ruiz, L.; Barriga, A.; Jerez, C.; Holmes, D.; Guiliani, N. C-di-GMP pathway in biomining bacteria. Adv. Mater. Res. 2009, 71–73, 223–226. [Google Scholar] [CrossRef]
  47. Fuqua, W.C.; Winans, S.C.; Greenberg, E.P. Quorum sensing in bacteria: The LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 1994, 176, 269–275. [Google Scholar] [CrossRef]
  48. Li, Z.; Nair, S.K. Quorum sensing: How bacteria can coordinate activity and synchronize their response to external signals? Protein Sci. 2012, 21, 1403–1417. [Google Scholar] [CrossRef]
  49. Sanders, J.G.; Akl, H.; Hagen, S.J.; Xue, B. Crosstalk enables mutual activation of coupled quorum sensing pathways through “jump-start” and “push-start” mechanisms. Sci. Rep. 2023, 13, 19230. [Google Scholar] [CrossRef]
  50. Mamani, S.; Moinier, D.; Denis, Y.; Soulère, L.; Queneau, Y.; Talla, E.; Bonnefoy, V.; Guiliani, N. Insights into the quorum sensing regulon of the acidophilic Acidithiobacillus ferrooxidans revealed by transcriptomic in the presence of an acyl homoserine lactone superagonist analog. Front. Microbiol. 2016, 7, 1365. [Google Scholar] [CrossRef]
  51. Banderas, A.; Guiliani, N. Bioinformatic prediction of gene functions regulated by quorum sensing in the bioleaching bacterium Acidithiobacillus ferrooxidans. Int. J. Mol. Sci. 2013, 14, 16901–16916. [Google Scholar] [CrossRef]
  52. Prescott, R.D.; Decho, A.W. Flexibility and Adaptability of Quorum Sensing in Nature. Trends Microbiol. 2020, 28, 436–444. [Google Scholar] [CrossRef]
  53. Parsek, M.R.; Val, D.L.; Hanzelka, B.L.; Cronan, J.E.; Greenberg, E.P. Acyl homoserine-lactone quorum-sensing signal generation. Proc. Natl. Acad. Sci. USA 1999, 96, 4360–4365. [Google Scholar] [CrossRef]
  54. Ortori, C.A.; Atkinson, S.; Chhabra, S.R.; Cámara, M.; Williams, P.; Barrett, D.A. Comprehensive profiling of N-acylhomoserine lactones produced by Yersinia pseudotuberculosis using liquid chromatography coupled to hybrid quadrupole–linear ion trap mass spectrometry. Anal. Bioanal. Chem. 2006, 387, 497–511. [Google Scholar] [CrossRef]
  55. Ruiz, L.; Gonzalez, A.R.; Frezza, M.; Soulère, L.; Queneau, Y.; Doutheau, A.; Rohwerder, T.; Sand, W.; Jerez, C.; Guiliani, N. Is the quorum sensing type AI-1 system of Acidithiobacillus ferrooxidans involved in its attachment to mineral surfaces? Adv. Mater. Res. 2007, 20–21, 345–349. [Google Scholar] [CrossRef]
  56. Churchill, M.E.A.; Chen, L. Structural basis of acyl-homoserine lactone-dependent signaling. Chem. Rev. 2011, 111, 68–85. [Google Scholar] [CrossRef] [PubMed]
  57. He, Y.-W.; Deng, Y.; Miao, Y.; Chatterjee, S.; Tran, T.M.; Tian, J.; Lindow, S. DSF-family quorum sensing signal-mediated intraspecies, interspecies, and inter-kingdom communication. Trends Microbiol. 2023, 31, 36–50. [Google Scholar] [CrossRef]
  58. Deng, Y.; Wu, J.; Tao, F.; Zhang, L.-H. Listening to a new language: DSF-based quorum sensing in gram-negative bacteria. Chem. Rev. 2011, 111, 160–173. [Google Scholar] [CrossRef] [PubMed]
  59. He, Y.W.; Wang, C.; Zhou, L.; Song, H.; Dow, J.M.; Zhang, L.H. Dual signaling functions of the hybrid sensor kinase RpfC of Xanthomonas campestris involve either phosphorelay or receiver domain-protein Interaction. J. Biol. Chem. 2006, 281, 33414–33421. [Google Scholar] [CrossRef] [PubMed]
  60. Lian, Z.; Chao, Y.L.; Yu, W.X.; Le, J.B.; Shuang, S.; Wen, H.Y. Identification and characterization of naturally occurring DSF-family quorum sensing signal turnover system in the phytopathogen Xanthomonas. Environ. Microbiol. 2015, 17, 4646–4658. [Google Scholar] [CrossRef]
  61. Bellenberg, S.; Buetti-Dinh, A.; Galli, V.; Ilie, O.; Herold, M.; Christel, S.; Boretska, M.; Pivkin, I.; Wilmes, P.; Sand, W.; et al. Automated microscopic analysis of metal sulfide colonization by acidophilic microorganisms. Appl. Environ. Microbiol. 2018, 84, e01835-18. [Google Scholar] [CrossRef] [PubMed]
  62. Christel, S.; Herold, M.; Bellenberg, S.; El Hajjami, M.; Buetti-Dinh, A.; Pivkin, I.V.; Sand, W.; Wilmes, P.; Poetsch, A.; Dopson, M. Multi-omics reveals the lifestyle of the acidophilic, mineral-oxidizing model species Leptospirillum ferriphilum(T). Appl. Environ. Microbiol. 2018, 84, e02091-17. [Google Scholar] [CrossRef]
  63. Moya-Beltrán, A.; Rojas-Villalobos, C.; Díaz, M.; Guiliani, N.; Quatrini, R.; Castro, M. Nucleotide second messenger-based signaling in extreme acidophiles of the Acidithiobacillus species complex: Partition between the core and variable gene complements. Front. Microbiol. 2019, 10, 381. [Google Scholar] [CrossRef]
  64. Díaz, M.; Guiliani, N. Molecular regulatory network involved in biofilm structure development by Acidithiobacillus thiooxidans includes Pel exopolysaccharide machinery. Solid State Phenom. 2017, 262, 330–333. [Google Scholar] [CrossRef]
  65. Chan, C.; Paul, R.; Samoray, D.; Amiot, N.C.; Giese, B.; Jenal, U.; Schirmer, T. Structural basis of activity and allosteric control of diguanylate cyclase. Proc. Natl. Acad. Sci. USA 2004, 101, 17084–17089. [Google Scholar] [CrossRef]
  66. Ryan, R.P. Cyclic di-GMP signalling and the regulation of bacterial virulence. Microbiology 2013, 159, 1286–1297. [Google Scholar] [CrossRef]
  67. Díaz, M.; Castro, M.; Copaja, S.; Guiliani, N. Biofilm formation by the acidophile bacterium Acidithiobacillus thiooxidans involves c-di-GMP pathway and Pel exopolysaccharide. Genes 2018, 9, 113. [Google Scholar] [CrossRef]
  68. Prentice, J.A.; Bridges, A.A.; Bassler, B.L. Synergy between c-di-GMP and quorum-sensing signaling in Vibrio cholerae biofilm morphogenesis. J. Bacteriol. 2022, 204, e0024922. [Google Scholar] [CrossRef]
  69. Lin, Y.; Mi, D.; Hou, Y.; Lin, M.; Xie, Q.; Niu, X.; Chen, Y.; He, C.; Tao, J.; Li, C. Systematic analysis of the roles of c-di-GMP signaling in Xanthomonas oryzae pv. oryzae virulence. FEMS Microbiol. Lett. 2022, 369, fnac068. [Google Scholar] [CrossRef]
  70. Ryan, R.P.; Fouhy, Y.; Lucey, J.F.; Jiang, B.L.; He, Y.Q.; Feng, J.X.; Tang, J.L.; Dow, J.M. Cyclic di-GMP signalling in the virulence and environmental adaptation of Xanthomonas campestris. Mol. Microbiol. 2006, 63, 429–442. [Google Scholar] [CrossRef]
  71. Galperin, M.Y.; Choub, S.-H. Sequence conservation, domain architectures, and phylogenetic distribution of the HD-GYP type c-di-GMP phosphodiesterases. J. Bacteriol. 2022, 204, e0056121. [Google Scholar] [CrossRef]
  72. Valdés, J.; Pedroso, I.; Quatrini, R.; Holmes, D. Comparative genome analysis of Acidithiobacillus ferrooxidans, A. thiooxidans and A. caldus: Insights into their metabolism and ecophysiology. Hydrometallurgy 2008, 94, 180–184. [Google Scholar] [CrossRef]
  73. Yang, C.L.; Chen, X.K.; Wang, R.; Lin, J.Q.; Liu, X.M.; Pang, X.; Zhang, C.J.; Lin, J.Q.; Chen, L. Essential role of σ Factor RpoF in flagellar biosynthesis and flagella-mediated motility of Acidithiobacillus caldus. Front. Microbiol. 2019, 10, 1130. [Google Scholar] [CrossRef]
  74. Feng, S.; Yang, H.; Xin, Y.; Zhang, L.; Kang, W.; Wang, W. Isolation of an extremely acidophilic and highly efficient strain Acidithiobacillus sp for chalcopyrite bioleaching. J. Ind. Microbiol. Biotechnol. 2012, 39, 1625–1635. [Google Scholar] [CrossRef]
  75. Xia, J.; Peng, A.; He, H.; Yang, Y.; Liu, X.; Qiu, G. A new strain Acidithiobacillus albertensis BY-05 for bioleaching of metal sulfides ores. Trans. Nonferrous Met. Soc. China 2007, 17, 168–175. [Google Scholar] [CrossRef]
  76. Yin, X.; Li, X.; Li, Q.; Wang, B.; Zheng, L. Complete genome analysis reveals environmental adaptability of sulfur-oxidizing bacterium Thioclava nitratireducens M1-LQ-LJL-11 and symbiotic relationship with deep-sea hydrothermal vent Chrysomallon squamiferum. Mar. Genom. 2023, 71, 101058. [Google Scholar] [CrossRef]
  77. Zeng, X.; Zou, Y.; Zheng, J.; Qiu, S.; Liu, L.; Wei, C. Quorum sensing-mediated microbial interactions: Mechanisms, applications, challenges and perspectives. Microbiol. Res. 2023, 273, 127414. [Google Scholar] [CrossRef]
  78. Lv, L.; Chen, J.; Liu, X.; Gao, W.; Sun, L.; Wang, P.; Ren, Z.; Zhang, G.; Li, W. Roles and regulation of quorum sensing in anaerobic granular sludge: Research status, challenges, and perspectives. Bioresour. Technol. 2023, 387, 129644. [Google Scholar] [CrossRef]
  79. Urvoy, M.; Lami, R.; Dreanno, C.; Delmas, D.; L’Helguen, S.; Labry, C. Quorum sensing regulates the hydrolytic enzyme production and community composition of heterotrophic bacteria in coastal waters. Front. Microbiol. 2021, 12, 780759. [Google Scholar] [CrossRef]
  80. Smith, P.; Schuster, M. Public goods and cheating in microbes. Curr. Biol. 2019, 29, R442–R447. [Google Scholar] [CrossRef]
  81. Zhao, K.; Liu, L.; Chen, X.; Huang, T.; Du, L.; Lin, J.; Yuan, Y.; Zhou, Y.; Yue, B.; Wei, K.; et al. Behavioral heterogeneity in quorum sensing can stabilize social cooperation in microbial populations. BMC Biol. 2019, 17, 20. [Google Scholar] [CrossRef]
  82. Mukherjee, S.; Bassler, B.L. Bacterial quorum sensing in complex and dynamically changing environments. Nat. Rev. Microbiol. 2019, 17, 371–382. [Google Scholar] [CrossRef]
  83. Rolland, J.L.; Stien, D.; Sanchez-Ferandin, S.; Lami, R. Quorum sensing and Quorum quenching in the phycosphere of phytoplankton: A case of chemical interactions in ecology. J. Chem. Ecol. 2016, 42, 1201–1211. [Google Scholar] [CrossRef]
  84. Mion, S.; Carriot, N.; Lopez, J.; Plener, L.; Ortalo-Magné, A.; Chabrière, E.; Culioli, G.; Daudé, D. Disrupting quorum sensing alters social interactions in Chromobacterium violaceum. npj Biofilms Microbiomes 2021, 7, 40. [Google Scholar] [CrossRef]
  85. Kaufmann, G.F.; Sartorio, R.; Lee, S.-H.; Rogers, C.J.; Meijler, M.M.; Moss, J.A.; Clapham, B.; Brogan, A.P.; Dickerson, T.J.; Janda, K.D. Revisiting quorum sensing: Discovery of additional chemical and biological functions for 3-oxo-N-acyl homoserine lactones. Proc. Natl. Acad. Sci. USA 2004, 102, 309–314. [Google Scholar] [CrossRef]
  86. Schertzer, J.W.; Boulette, M.L.; Whiteley, M. More than a signal: Non-signaling properties of quorum sensing molecules. Trends Microbiol. 2009, 17, 189–195. [Google Scholar] [CrossRef]
  87. Parsons, J.B.; Yao, J.; Frank, M.W.; Jackson, P.; Rock, C.O. Membrane disruption by antimicrobial fatty acids releases low-molecular-weight proteins from Staphylococcus aureus. J. Bacteriol. 2012, 194, 5294–5304. [Google Scholar] [CrossRef]
  88. Shen, L.; Cheng, J.; Wang, J.; Zhang, Y.; Zhou, H.; Wu, X.; Li, J.; Zeng, W. Biofilm formation and development during the pyrite bioleaching of moderately thermophilic microorganisms. Hydrometallurgy 2023, 222, 106183. [Google Scholar] [CrossRef]
  89. Recalde, A.; Gonzalez-Madrid, G.; Acevedo-Lopez, J.; Jerez, C.A. Sessile lifestyle offers protection against copper stress in Saccharolobus solfataricus. Microorganisms 2023, 11, 1421. [Google Scholar] [CrossRef]
  90. Zhang, R.; Neu, T.; Blanchard, V.; Vera, M.; Sand, W. Biofilm dynamics and EPS production of a thermoacidophilic bioleaching archaeon. New Biotechnol. 2019, 51, 21–30. [Google Scholar] [CrossRef] [PubMed]
  91. van Alin, A.; Corbett, M.K.; Fathollahzadeh, H.; Tjiam, M.C.; Rickard, W.D.A.; Sun, X.; Putnis, A.; Eksteen, J.; Kaksonen, A.H.; Watkin, E. Biofilm formation on the surface of monazite and xenotime during bioleaching. Microb. Biotechnol. 2023, 16, 1790–1802. [Google Scholar] [CrossRef] [PubMed]
  92. Salinas, J.I.; Nunez-Ramirez, D.M.; Manero, O.; Bautista, F.; Medina-Torres, L. Modeling of the bioleaching of process silver pulp. Chem. Eng. Technol. 2023, 47, 396–402. [Google Scholar] [CrossRef]
  93. Donlan, R.M. Biofilms: Microbial life on surfaces. Emerg. Infect. Dis. 2002, 8, 881–890. [Google Scholar] [CrossRef]
  94. Kostakioti, M.; Hadjifrangiskou, M.; Hultgren, S.J. Bacterial biofilms: Development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harb. Perspect. Med. 2013, 3, a010306. [Google Scholar] [CrossRef] [PubMed]
  95. Marshall, K.C.; Stout, R.; Mitchell, R. Mechanism of the initial events in the sorption of marine bacteria to surfaces. J. Gen. Microbiol. 1971, 68, 337–348. [Google Scholar] [CrossRef]
  96. Toyofuku, M.; Inaba, T.; Kiyokawa, T.; Obana, N.; Yawata, Y.; Nomura, N. Environmental factors that shape biofilm formation. Biosci. Biotechnol. Biochem. 2016, 80, 7–12. [Google Scholar] [CrossRef]
  97. Hu, W.; Feng, S.; Tong, Y.; Zhang, H.; Yang, H. Adaptive defensive mechanism of bioleaching microorganisms under extremely environmental acid stress: Advances and perspectives. Biotechnol. Adv. 2020, 42, 107580. [Google Scholar] [CrossRef]
  98. Gonzalez, A.R.; Bellenberg, S.; Mamani, S.; Ruiz, L.; Echeverría, A.; Soulère, L.; Doutheau, A.; Demergasso, C.; Sand, W.; Queneau, Y.; et al. AHL signaling molecules with a large acyl chain enhance biofilm formation on sulfur and metal sulfides by the bioleaching bacterium Acidithiobacillus ferrooxidans. Appl. Microbiol. Biotechnol. 2013, 97, 3729–3737. [Google Scholar] [CrossRef] [PubMed]
  99. Castro, M.; Díaz, M.; Beltrán, A.M.; Guiliani, N. Cyclic di-GMP signaling in extreme acidophilic bacteria. In Microbial Cyclic Di-Nucleotide Signaling; Chou, S., Guiliani, N., Lee, V., Römling, U., Eds.; Springer: Cham, Switzerland, 2020; pp. 337–353. [Google Scholar]
  100. Castro, M.; Deane, S.; Ruiz, L.; Rawlings, D.; Guiliani, N. Diguanylate cyclase null mutant reveals that c-di-GMP pathway regulates the motility and adherence of the extremophile bacterium Acidithiobacillus caldus. PLoS ONE 2015, 10, e0116399. [Google Scholar] [CrossRef]
  101. Ranava, D.; Backes, C.; Karthikeyan, G.; Ouari, O.; Soric, A.; Guiral, M.; Cardenas, M.L.; Giudici-Orticoni, M.T. Metabolic exchange and energetic coupling between nutritionally stressed bacterial species: Role of quorum-sensing molecules. mBio 2021, 12, e02758-20. [Google Scholar] [CrossRef]
  102. Liu, Y.; Gao, J.; Wang, N.; Li, X.; Fang, N.; Zhuang, X. Diffusible signal factor enhances the saline-alkaline resistance and rhizosphere colonization of Stenotrophomonas rhizophila by coordinating optimal metabolism. Sci. Total Environ. 2022, 834, 155403. [Google Scholar] [CrossRef]
  103. Li, J.; Liu, H.; Zhao, C.; Zhang, J.; He, W. Autoinducer-2 quorum sensing regulates biofilm formation and chain elongation metabolic pathways to enhance caproate synthesis in microbial electrochemical system. Chemosphere 2023, 344, 140384. [Google Scholar] [CrossRef]
  104. Gao, X.Y.; Fu, C.A.; Hao, L.; Gu, X.; Wang, R.; Lin, J.Q.; Liu, X.M.; Pang, X.; Zhang, C.J.; Lin, J.Q.; et al. The substrate-dependent regulatory effects of the AfeI/R system in Acidithiobacillus ferrooxidans reveals the novel regulation strategy of quorum sensing in acidophiles. Environ. Microbiol. 2020, 23, 757–773. [Google Scholar] [CrossRef]
  105. Li, Y.; Wang, S.; Ding, H.; Xiao, K.; Huang, X. Quorum sensing-Fe metabolism interplay affects biofouling on reverse osmosis membrane: Evidences from microbial shift and structure alteration. Desalination 2023, 551, 116416. [Google Scholar] [CrossRef]
  106. Gao, X.Y.; Liu, X.; Fu, C.A.; Gu, X.; Lin, J.; Liu, X.M.; Pang, X.; Lin, J.Q.; Chen, L. Novel strategy for improvement of the bioleaching efficiency of Acidithiobacillus ferrooxidans based on the AfeI/R quorum sensing system. Minerals 2020, 10, 222. [Google Scholar] [CrossRef]
  107. Jung, H.; Inaba, Y.; West, A.; Banta, S. Overexpression of quorum sensing genes in Acidithiobacillus ferrooxidans enhances cell attachment and covellite bioleaching. Biotechnol. Rep. 2023, 38, e00789. [Google Scholar] [CrossRef] [PubMed]
  108. Bellenberg, S.; Barthen, R.; Vera, M.; Guiliani, N.; Sand, W. Biofilm formation, communication and interactions of mesophilic leaching bacteria during pyrite oxidation. Adv. Mater. Res. 2013, 825, 107–110. [Google Scholar] [CrossRef]
  109. Mamani, S.; Denis, Y.; Moinier, D.; Sabbah, M.; Soulère, L.; Queneau, Y.; Bonnefoy, V.; Guiliani, N. Characterization of the quorum sensing regulon in Acidithiobacillus ferrooxidans. Adv. Mater. Res. 2013, 825, 129–132. [Google Scholar] [CrossRef]
  110. Lv, L.; Li, W.; Zheng, Z.; Li, D.; Zhang, N. Exogenous acyl-homoserine lactones adjust community structures of bacteria and methanogens to ameliorate the performance of anaerobic granular sludge. J. Hazard. Mater. 2018, 354, 72–80. [Google Scholar] [CrossRef] [PubMed]
  111. Li, Y.S.; Pan, X.R.; Cao, J.S.; Song, X.N.; Fang, F.; Tong, Z.H.; Li, W.W.; Yu, H.Q. Augmentation of acyl homoserine lactones-producing and -quenching bacterium into activated sludge for its granulation. Water Res. 2017, 125, 309–317. [Google Scholar] [CrossRef]
  112. Wang, J.; Liu, Q.; Li, X.; Ma, S.; Hu, H.; Wu, B.; Zhang, X.X.; Ren, H. In-situ monitoring AHL-mediated quorum-sensing regulation of the initial phase of wastewater biofilm formation. Environ. Int. 2020, 135, 105326. [Google Scholar] [CrossRef]
  113. Xiong, F.; Zhao, X.; Wen, D.; Li, Q. Effects of N-acyl-homoserine lactones-based quorum sensing on biofilm formation, sludge characteristics, and bacterial community during the start-up of bioaugmented reactors. Sci. Total Environ. 2020, 735, 139449. [Google Scholar] [CrossRef]
  114. Lv, L.; Feng, C.; Li, W.; Zhang, G.; Wang, P.; Ren, Z. Exogenous N-acyl-homoserine lactones promote the degradation of refractory organics in oligotrophic anaerobic granular sludge. Sci. Total Environ. 2021, 761, 143289. [Google Scholar] [CrossRef]
  115. Liu, R.; Chen, J.; Zhou, W.; Cheng, H.; Zhou, H. Insight to the early-stage adsorption mechanism of moderately thermophilic consortia and intensified bioleaching of chalcopyrite. Biochem. Eng. J. 2019, 144, 40–47. [Google Scholar] [CrossRef]
  116. Zeng, W.; Liu, Z.; Amanze, C.; Cheng, J.; Liao, W.; Wu, X.-L.; Qiu, G.; Wang, Q.; Wu, Z.; Zou, L.; et al. In situ detection of Cu2+, Fe3+ and Fe2+ ions at the microbe-mineral interface during bioleaching of chalcopyrite by moderate thermophiles. Miner. Eng. 2023, 191, 107936. [Google Scholar] [CrossRef]
  117. Moncayo, E.A.; Debut, A.; Vizuete, K.; Jumbo-Flores, D.; Aguirre, P. Sticky bacteria: Combined effect of galactose and high ferric iron concentration on extracellular polymeric substances production and the attachment of Acidithiobacillus ferrooxidans on a polymetallic sulfide ore surface. Front. Microbiol. 2022, 13, 951402. [Google Scholar] [CrossRef]
  118. Zeng, W.M.; Cai, Y.X.; Hou, C.W.; Liu, A.j.; Peng, T.J.; Chen, M.; Qiu, G.Z.; Shen, L. Influence diversity of extracellular DNA on bioleaching chalcopyrite and pyrite by Sulfobacillus thermosulfidooxidans ST. J. Cent. South Univ. 2020, 27, 1466–1476. [Google Scholar] [CrossRef]
  119. Ning, X.J.; Ying, Y.H.; Lin, T.L. Adsorption behavior of glucuronic acid on pyrite surface: An electrochemical and DFT study. Arch. Metall. Mater. 2020, 65, 433–440. [Google Scholar] [CrossRef]
  120. Chu, H.; Wang, J.; Tian, B.; Qian, C.; Niu, T.; Qi, S.; Yang, Y.; Ge, Y.; Dai, X.; Xin, B. Generation behavior of extracellular polymeric substances and its correlation with extraction efficiency of valuable metals and change of process parameters during bioleaching of spent petroleum catalyst. Chemosphere 2021, 275, 130006. [Google Scholar] [CrossRef]
  121. Ma, C.; Zeng, W.; Meng, Q.; Wang, C.; Peng, Y. Identification of partial denitrification granulation enhanced by low C/N ratio in the aspect of metabolomics and quorum sensing. Chemosphere 2022, 286, 131895. [Google Scholar] [CrossRef]
  122. Chabert, N.; Bonnefoy, V.; Achouak, W. Quorum sensing improves current output with Acidithiobacillus ferrooxidans. Microb. Biotechnol. 2017, 11, 136–140. [Google Scholar] [CrossRef]
  123. Caicedo, J.C.; Villamizar, S.; Orlandoni, G. The use of synthetic agonists of quorum sensing N- acyl homoserine lactone pathway improves the bioleaching ability in Acidithiobacillus and Pseudomonas bacteria. PeerJ 2022, 10, e13801. [Google Scholar] [CrossRef] [PubMed]
  124. Liu, L.; Zeng, X.; Zheng, J.; Zou, Y.; Qiu, S.; Dai, Y. AHL-mediated quorum sensing to regulate bacterial substance and energy metabolism: A review. Microbiol. Res. 2022, 262, 127102. [Google Scholar] [CrossRef] [PubMed]
Microorganisms 12 00422 g001
Figure 1. Regulation mechanism of bioleaching based on quorum sensing. QS has been extensively studied and proven to affect various aspects of cell morphology, community structure, biofilm formation, and cell metabolism in regulating the bioleaching process. Acronyms: SAM = S-adenosyl-L-methionine, EPS = extracellular polymers.
Figure 1. Regulation mechanism of bioleaching based on quorum sensing. QS has been extensively studied and proven to affect various aspects of cell morphology, community structure, biofilm formation, and cell metabolism in regulating the bioleaching process. Acronyms: SAM = S-adenosyl-L-methionine, EPS = extracellular polymers.
Microorganisms 12 00422 g001
Table 1. Iron–sulfur oxidizing microorganisms in bioleaching.
Table 1. Iron–sulfur oxidizing microorganisms in bioleaching.
(a) iron metabolism
MicroorganismsRegulatory genesEnzymeElectron transfer chainReferences
Acidithiobacillus ferrooxidans ATCC 23270rusA/BRusticyanin oxidase1. Fe2+ → Rusticyanin oxidase → Cyc1 → aa3 oxidase
2. Fe2+ → Rusticyanin oxidase → CycA1 → bc1 complex
3. Fe2+→Cyt579 → Cytochrome c		[6,19,20,21,22]
iroIron oxidase
A. ferrivorans s DSM 22755fox clusterhaem–copper terminal
Leptospirillum ferriphilum DSM 17947 Cyc1
Sulfobacillus acidophilus DSM 10332 CycA1
Sulfolobus tokodaii JCM10545
Acidiplasma aeolicum DSM 18409
Acidianus brierleyi DSM 1651
Metallosphaera sedula DSM 5348		 Cyt579
(b) sulfur metabolism
MicroorganismsRegulatory genesEnzymeReactionReferences
Acidithiobacillus caldus ATCC 51756
A. thiobacillus A01
A. ferrooxidans ATCC 23270
A. ferrivorans DSM 22755
Sulfobacillus acidophilus DSM 10332
Acidianus copahuensis ALE1
Metallosphaera sedula DSM 535		tetHTetrathionate hydrolaseS4O62− → S2O32− + SO42− + S0
tsdThiosulfate dehydrogenaseS2O32− → S4O62−
sqrSulfide quinone reductaseH2S → S0[19,20,23,24,25]
doxDAThiosulfate: quinone oxidoreductaseS2O32− → S4O62–
sorSulfur oxygenase reductaseS0 → H2S + SO32− + S2O32–
tstThiosulfate sulfurtransferase S2O32− → SO32− + S0
hdrABCHeterodisulfide reductase complex glutathione oxidized → glutathione + SO3 2−
sat/cysCSulfate adenylyltransferase/adenylylsulfate kinaseadenosine phosphosulfate → SO42−
sarsulfite: acceptor oxidoreductaseSO3 2− → SO42−
SoxXYZABSox systemS2−/S0/S2O32−/SO32− → SO4 2−
Table 2. Structure and function of major AIs in acidophiles. Acronyms: AIs = autoinducers, DGCs = diguanylate cyclases, PDEs = phosphodiesterases, AHLs = N-acyl-homoserine lactones, DSFs = diffusible signal factor, c-di-GMP = cyclic dimeric guanosine monophosphate.
Table 2. Structure and function of major AIs in acidophiles. Acronyms: AIs = autoinducers, DGCs = diguanylate cyclases, PDEs = phosphodiesterases, AHLs = N-acyl-homoserine lactones, DSFs = diffusible signal factor, c-di-GMP = cyclic dimeric guanosine monophosphate.
AIsMicroorganismsTypical StructuresRegulatory ProteinsFunctionsReferences
AHLsA. ferrooxidans ATCC 23270
A. thiooxidans DSMZ 504
L. ferrooxidans DSM 2391 *
A. ferrivorans SS3 *		Microorganisms 12 00422 i001LuxI
LuxR
Act		1. Biofilm formation
2. Protein secretion
3. Flagellar movement		[17,38,39,43,44,45]
DSFL. ferrooxidans DSM 2705
L. ferriphilum DSM 14647		Microorganisms 12 00422 i002RpfG
RpfF
RpfC		1. Biofilm formation
2. Resistance
[40]
c-di-GMPA. ferrooxidans ATCC 23270
A. thiooxidans ATCC 51756
A. caldus ATCC 19377		Microorganisms 12 00422 i003DGCs
PDEs		1. Flagellar movement
2. Substrate adhesion
3. Biofilm formation		[46]
* indicates that the bacterium only contains orphan receptors.
Table 3. Quorum sensing-based exogenous regulation in acidophiles. Acronyms: HSL = homoserine lactone, OH-HSL = hydroxy-homoserine lactone, oxo-HSL = oxygen-homoserine lactone, 3-oxo-C8-HSL = N-(3-Oxooctanoyl)-L-homoserine lactone, BDSF = Burkholderia diffusible signal factor ((Z)-2-dodecenoic acid).
Table 3. Quorum sensing-based exogenous regulation in acidophiles. Acronyms: HSL = homoserine lactone, OH-HSL = hydroxy-homoserine lactone, oxo-HSL = oxygen-homoserine lactone, 3-oxo-C8-HSL = N-(3-Oxooctanoyl)-L-homoserine lactone, BDSF = Burkholderia diffusible signal factor ((Z)-2-dodecenoic acid).
Exogenous MoleculesAcidophilesSubstrateResultsReferences
OH-HSLs + oxo-HSLs A. ferrooxidans ATCC 23270pyritereduce adhesion[55]
-HSL + OH-HSLA. ferrooxidans ATCC 23270sulfur increase attachment[98]
-HSL + OH-HSL + oxo-HSL/C14-HSLA. ferrooxidans ATCC 23270sulfur/pyritepromote biofilm formation[98]
-HSL + oxo -HSLs + OH -HSLA. ferrivorans SS3pyrite1. inhibit biofilm formation 2. reduce the leaching rate[108]
-HSL + oxo-HSL + OH-HSLL. ferrooxidans DSM 2391pyrite1. inhibit biofilm formation 2. reduce the leaching rate[108]
C8-HSL/3-oxo-C8-HSL/C10-HSLA. thiooxidans DSM 14887sulfur promote biofilm formation[17]
3-sulfonylamide-C8-HSLA. ferrooxidans ATCC 23270pyriteincrease attachment[55]
4-phenyl-3-oxo-HSLA. ferrooxidans ATCC 23270pyritereduce adhesion[55]
tetrazoleA. ferrooxidans ATCC 23270sulfur 1. increase attachment
2. up-regulate afeI and zwf gene expression		[109]
tetrazole 9cA. ferrooxidans ATCC 23270sulfur increase attachment[50]
DSF + BDSFL. ferriphilum DSM 14647Fe2+/pyrite1. inhibit iron oxidation
2. reduce adhesion		[40,61]
DSF + BDSFS. thermosulfidooxidans DSM 9293Fe2+/pyrite1. inhibit iron oxidation
2. reduce adhesion		[40,61]
DSF + BDSFA. ferrooxidans ATCC 23270Fe2+inhibit iron oxidation[40,61]
DSF + BDSFA. caldus DSM 8584pyritereduce adhesion[61]
DSF/BDSF + AHLL. ferriphilum DSM 14647Fe2+reduce flrB transcription levels[40]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Luo, W.; Li, Y.; Chen, S.; Liang, Y.; Liu, X. Roles and Regulation of Quorum Sensing of Acidophiles in Bioleaching: A Review. Microorganisms 2024, 12, 422. https://doi.org/10.3390/microorganisms12030422

AMA Style

Luo W, Li Y, Chen S, Liang Y, Liu X. Roles and Regulation of Quorum Sensing of Acidophiles in Bioleaching: A Review. Microorganisms. 2024; 12(3):422. https://doi.org/10.3390/microorganisms12030422

Chicago/Turabian Style

Luo, Wang, Yiran Li, Shiqi Chen, Yili Liang, and Xueduan Liu. 2024. "Roles and Regulation of Quorum Sensing of Acidophiles in Bioleaching: A Review" Microorganisms 12, no. 3: 422. https://doi.org/10.3390/microorganisms12030422

APA Style

Luo, W., Li, Y., Chen, S., Liang, Y., & Liu, X. (2024). Roles and Regulation of Quorum Sensing of Acidophiles in Bioleaching: A Review. Microorganisms, 12(3), 422. https://doi.org/10.3390/microorganisms12030422

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop