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Mechanisms of Microbial Adaptation to Low pH
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Mechanisms of Microbial Adaptation to Low pH

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Microbial Genetics and Genomics".

Deadline for manuscript submissions: closed (30 September 2020) | Viewed by 31858

Special Issue Editors

Prof. Dr. Daniela De Biase

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Guest Editor
Department of Medico-Surgical Sciences and Biotechnologies, Sapienza University of Rome, Latina, Italy
Interests: Escherichia coli; glutamate decarboxylase; amino acid-dependent acid resistance; GABA
Prof. Dr. Nuno Pereira Mira

E-Mail Website
Guest Editor
Institute for Bioengineering and Biosciences; Instituto Superior Técnico, Department of Bioengineering; University of Lisbon, 1649-004 Lisboa, Portugal
Interests: yeasts genomics and physiology; antinfungal resistance in Candida spp; transcriptional regulatory networks
Dr. Peter A. Lund

E-Mail Website
Guest Editor
Institute of Microbiolgy and Infection, School of Biosciences, University of Birmingham, Birmingham B15 2TT, UK
Interests: bacterial stress responses; acid stress; laboratory-based evolution; molecualr chaperones

Special Issue Information

Dear Colleagues,

The adaptation of microorganisms to low pH has many important practical applications in a number of diverse sectors such as food and drink microbiology, industrial biotechnology and bio-processing, and clinical and veterinary treatment of infections, in a time of increasing antimicrobial resistance. The microorganisms under consideration include bacteria, yeasts, and other fungi. With this Special Issue, we aim to collect high-quality research articles describing the genomic, transcriptomic, sensing, and metabolic landscape of the microbial responses to low pH with a view to understanding their functional significance and bridging to potential applications gathered from the covered knowledge. We wish to cover all aspects of the molecular events from sensing to responding to low pH stress, and also to cover descriptions of genes in different organisms that may have specific functions at low pH. Adaptation is therefore meant both in terms of the short-term response, and also in the description of how evolution has enabled microorganisms to be resilient to acid stress. This is in line with the objectives of the COST Action “EuroMicropH” (https://euromicroph.eu), which is committed to aiding the understanding of the details of how model and non-model micro-organisms detect and respond to low pH.

Prof. Daniela De Biase
Dr. Peter A. Lund
Prof. Nuno Pereira Mira
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Genes is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • microbial physiology
  • weak organic acids
  • acid stress responses
  • low pH sensing
  • omics approaches

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Published Papers (6 papers)

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Research

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25 pages, 12425 KiB  
Article
Mapping the Transcriptional and Fitness Landscapes of a Pathogenic E. coli Strain: The Effects of Organic Acid Stress under Aerobic and Anaerobic Conditions
by Francesca Bushell, John M. J. Herbert, Thippeswamy H. Sannasiddappa, Daniel Warren, A. Keith Turner, Francesco Falciani and Peter A. Lund
Genes 2021, 12(1), 53; https://doi.org/10.3390/genes12010053 - 31 Dec 2020
Cited by 5 | Viewed by 4121
Abstract
Several methods are available to probe cellular responses to external stresses at the whole genome level. RNAseq can be used to measure changes in expression of all genes following exposure to stress, but gives no information about the contribution of these genes to [...] Read more.
Several methods are available to probe cellular responses to external stresses at the whole genome level. RNAseq can be used to measure changes in expression of all genes following exposure to stress, but gives no information about the contribution of these genes to an organism’s ability to survive the stress. The relative contribution of each non-essential gene in the genome to the fitness of the organism under stress can be obtained using methods that use sequencing to estimate the frequencies of members of a dense transposon library grown under different conditions, for example by transposon-directed insertion sequencing (TraDIS). These two methods thus probe different aspects of the underlying biology of the organism. We were interested to determine the extent to which the data from these two methods converge on related genes and pathways. To do this, we looked at a combination of biologically meaningful stresses. The human gut contains different organic short-chain fatty acids (SCFAs) produced by fermentation of carbon compounds, and Escherichia coli is exposed to these in its passage through the gut. Their effect is likely to depend on both the ambient pH and the level of oxygen present. We, therefore, generated RNAseq and TraDIS data on a uropathogenic E. coli strain grown at either pH 7 or pH 5.5 in the presence or absence of three SCFAs (acetic, propionic and butyric), either aerobically or anaerobically. Our analysis identifies both known and novel pathways as being likely to be important under these conditions. There is no simple correlation between gene expression and fitness, but we found a significant overlap in KEGG pathways that are predicted to be enriched following analysis of the data from the two methods, and the majority of these showed a fitness signature that would be predicted from the gene expression data, assuming expression to be adaptive. Genes which are not in the E. coli core genome were found to be particularly likely to show a positive correlation between level of expression and contribution to fitness. Full article
(This article belongs to the Special Issue Mechanisms of Microbial Adaptation to Low pH)
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17 pages, 2794 KiB  
Article
Carbon Source Influence on Extracellular pH Changes along Bacterial Cell-Growth
by Rubén Sánchez-Clemente, M. Isabel Guijo, Juan Nogales and Rafael Blasco
Genes 2020, 11(11), 1292; https://doi.org/10.3390/genes11111292 - 30 Oct 2020
Cited by 32 | Viewed by 5228
Abstract
The effect of initial pH on bacterial cell-growth and its change over time was studied under aerobic heterotrophic conditions by using three bacterial strains: Escherichia coli ATCC 25922, Pseudomonas putida KT2440, and Pseudomonas pseudoalcaligenes CECT 5344. In Luria-Bertani (LB) media, pH evolved by [...] Read more.
The effect of initial pH on bacterial cell-growth and its change over time was studied under aerobic heterotrophic conditions by using three bacterial strains: Escherichia coli ATCC 25922, Pseudomonas putida KT2440, and Pseudomonas pseudoalcaligenes CECT 5344. In Luria-Bertani (LB) media, pH evolved by converging to a certain value that is specific for each bacterium. By contrast, in the buffered Minimal Medium (MM), pH was generally more stable along the growth curve. In MM with glucose as carbon source, a slight acidification of the medium was observed for all strains. In the case of E. coli, a sudden drop in pH was observed during exponential cell growth that was later recovered at initial pH 7 or 8, but was irreversible below pH 6, thus arresting further cell-growth. When using other carbon sources in MM at a fixed initial pH, pH changes depended mainly on the carbon source itself. While glucose, glycerol, or octanoate slightly decreased extracellular pH, more oxidized carbon sources, such as citrate, 2-furoate, 2-oxoglutarate, and fumarate, ended up with the alkalinization of the medium. These observations are in accordance with pH change predictions using genome-scale metabolic models for the three strains, thus revealing the metabolic reasons behind pH change. Therefore, we conclude that the composition of the medium, specifically the carbon source, determines pH change during bacterial growth to a great extent and unravel the main molecular mechanism behind this phenotype. These findings pave the way for predicting pH changes in a given bacterial culture and may anticipate the interspecies interactions and fitness of bacteria in their environment. Full article
(This article belongs to the Special Issue Mechanisms of Microbial Adaptation to Low pH)
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15 pages, 1346 KiB  
Article
The Acidic Stress Response of the Intracellular Pathogen Brucella melitensis: New Insights from a Comparative, Genome-Wide Transcriptome Analysis
by David Kornspan, Tamar Zahavi and Mali Salmon-Divon
Genes 2020, 11(9), 1016; https://doi.org/10.3390/genes11091016 - 28 Aug 2020
Viewed by 3256
Abstract
The intracellular pathogenic bacteria belonging to the genus Brucella must cope with acidic stress as they penetrate the host via the gastrointestinal route, and again during the initial stages of intracellular infection. A transcription-level regulation has been proposed to explain this but the [...] Read more.
The intracellular pathogenic bacteria belonging to the genus Brucella must cope with acidic stress as they penetrate the host via the gastrointestinal route, and again during the initial stages of intracellular infection. A transcription-level regulation has been proposed to explain this but the specific molecular mechanisms are yet to be determined. We recently reported a comparative transcriptomic analysis of the attenuated vaccine Brucella melitensis strain Rev.1 against the virulent strain 16M in cultures grown under either neutral or acidic conditions. Here, we re-analyze the RNA-seq data of 16M from our previous study and compare it to published transcriptomic data of this strain from both an in cellulo and an in vivo model. We identify 588 genes that are exclusively differentially expressed in 16M grown under acidic versus neutral pH conditions, including 286 upregulated genes and 302 downregulated genes that are not differentially expressed in either the in cellulo or the in vivo model. Of these, we highlight 13 key genes that are known to be associated with a bacterial response to acidic stress and, in our study, were highly upregulated under acidic conditions. These genes provide new molecular insights into the mechanisms underlying the acid-resistance of Brucella within its host. Full article
(This article belongs to the Special Issue Mechanisms of Microbial Adaptation to Low pH)
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19 pages, 1911 KiB  
Article
Escherichia coli Increases its ATP Concentration in Weakly Acidic Environments Principally through the Glycolytic Pathway
by Wenbin Zhang, Xin Chen, Wei Sun, Tao Nie, Natalie Quanquin and Yirong Sun
Genes 2020, 11(9), 991; https://doi.org/10.3390/genes11090991 - 25 Aug 2020
Cited by 28 | Viewed by 5758
Abstract
Acid resistance is an intrinsic characteristic of intestinal bacteria in order to survive passage through the stomach. Adenosine triphosphate (ATP), the ubiquitous chemical used to power metabolic reactions, activate signaling cascades, and form precursors of nucleic acids, was also found to be associated [...] Read more.
Acid resistance is an intrinsic characteristic of intestinal bacteria in order to survive passage through the stomach. Adenosine triphosphate (ATP), the ubiquitous chemical used to power metabolic reactions, activate signaling cascades, and form precursors of nucleic acids, was also found to be associated with the survival of Escherichia coli (E. coli) in acidic environments. The metabolic pathway responsible for elevating the level of ATP inside these bacteria during acid adaptation has been unclear. E. coli uses several mechanisms of ATP production, including oxidative phosphorylation, glycolysis and the oxidation of organic compounds. To uncover which is primarily used during adaptation to acidic conditions, we broadly analyzed the levels of gene transcription of multiple E. coli metabolic pathway components. Our findings confirmed that the primary producers of ATP in E. coli undergoing mild acidic stress are the glycolytic enzymes Glk, PykF and Pgk, which are also essential for survival under markedly acidic conditions. By contrast, the transcription of genes related to oxidative phosphorylation was downregulated, despite it being the major producer of ATP in neutral pH environments. Full article
(This article belongs to the Special Issue Mechanisms of Microbial Adaptation to Low pH)
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25 pages, 3924 KiB  
Article
Extreme Low Cytosolic pH Is a Signal for Cell Survival in Acid Stressed Yeast
by Rodrigo Mendonça Lucena, Laura Dolz-Edo, Stanley Brul, Marcos Antonio de Morais, Jr. and Gertien Smits
Genes 2020, 11(6), 656; https://doi.org/10.3390/genes11060656 - 16 Jun 2020
Cited by 21 | Viewed by 5715
Abstract
Yeast biomass is recycled in the process of bioethanol production using treatment with dilute sulphuric acid to control the bacterial population. This treatment can lead to loss of cell viability, with consequences on the fermentation yield. Thus, the aim of this study was [...] Read more.
Yeast biomass is recycled in the process of bioethanol production using treatment with dilute sulphuric acid to control the bacterial population. This treatment can lead to loss of cell viability, with consequences on the fermentation yield. Thus, the aim of this study was to define the functional cellular responses to inorganic acid stress. Saccharomyces cerevisiae strains with mutation in several signalling pathways, as well as cells expressing pH-sensitive GFP derivative ratiometric pHluorin, were tested for cell survival and cytosolic pH (pHc) variation during exposure to low external pH (pHex). Mutants in calcium signalling and proton extrusion were transiently sensitive to low pHex, while the CWI slt2Δ mutant lost viability. Rescue of this mutant was observed when cells were exposed to extreme low pHex or glucose starvation and was dependent on the induced reduction of pHc. Therefore, a lowered pHc leads to a complete growth arrest, which protects the cells from lethal stress and keeps cells alive. Cytosolic pH is thus a signal that directs the growth stress-tolerance trade-off in yeast. A regulatory model was proposed to explain this mechanism, indicating the impairment of glucan synthesis as the primary cause of low pHex sensitivity. Full article
(This article belongs to the Special Issue Mechanisms of Microbial Adaptation to Low pH)
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Review

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21 pages, 9029 KiB  
Review
Comparative Review of the Responses of Listeria monocytogenes and Escherichia coli to Low pH Stress
by Talia Arcari, Marie-Lucie Feger, Duarte N. Guerreiro, Jialun Wu and Conor P. O’Byrne
Genes 2020, 11(11), 1330; https://doi.org/10.3390/genes11111330 - 11 Nov 2020
Cited by 52 | Viewed by 6416
Abstract
Acidity is one of the principal physicochemical factors that influence the behavior of microorganisms in any environment, and their response to it often determines their ability to grow and survive. Preventing the growth and survival of pathogenic bacteria or, conversely, promoting the growth [...] Read more.
Acidity is one of the principal physicochemical factors that influence the behavior of microorganisms in any environment, and their response to it often determines their ability to grow and survive. Preventing the growth and survival of pathogenic bacteria or, conversely, promoting the growth of bacteria that are useful (in biotechnology and food production, for example), might be improved considerably by a deeper understanding of the protective responses that these microorganisms deploy in the face of acid stress. In this review, we survey the molecular mechanisms used by two unrelated bacterial species in their response to low pH stress. We chose to focus on two well-studied bacteria, Escherichia coli (phylum Proteobacteria) and Listeria monocytogenes (phylum Firmicutes), that have both evolved to be able to survive in the mammalian gastrointestinal tract. We review the mechanisms that these species use to maintain a functional intracellular pH as well as the protective mechanisms that they deploy to prevent acid damage to macromolecules in the cells. We discuss the mechanisms used to sense acid in the environment and the regulatory processes that are activated when acid is encountered. We also highlight the specific challenges presented by organic acids. Common themes emerge from this comparison as well as unique strategies that each species uses to cope with acid stress. We highlight some of the important research questions that still need to be addressed in this fascinating field. Full article
(This article belongs to the Special Issue Mechanisms of Microbial Adaptation to Low pH)
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