On the Microbe-Essential Oil Interplay: Processes, Mechanisms, Impacts and Applications

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Phytochemistry".

Deadline for manuscript submissions: closed (15 March 2023) | Viewed by 15447

Special Issue Editor


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Guest Editor
Department of Ecology, School of Biology, UPB 119, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
Interests: plant–microbe interactions; aerobiology; plant phenology; allelopathy; conservation; aromatic plants; essential oils; Mediterranean ecosystems; protected areas; environmental education

Special Issue Information

Dear Colleagues,

With more than six thousand years of continuous use, essential oils are amongst the most ancient plant-derived, non-food products in the service of humankind. Artifacts, inscriptions, and manuscripts from Egypt, Mesopotamia, China, India, and Greece show that they have played an important role in the life of people since early human civilization, serving their spiritual and physical needs: to honor their gods, to embalm the dead, to cure and perfume themselves, etc. Their use continues uninterrupted to this day. Along with scent, antimicrobial activity has been their most valued property. A large number of studies show this activity to be expressed against bacteria, fungi, viruses, and many invertebrates which are invisible to the naked eye—microbes sensu lato (e.g., mites), along with other activities like antifeedant, insecticidal, or allelopathic. As expected, such inhibitory effects are not universal. We know insects are attracted by flowers’ scent, fungi sporulate intensely in the presence of essential oils, bacteria proliferate next to the glandular hairs of the leaves of Lamiaceae representatives, and weeds grow in abundance in cultivations of aromatic plants. Many other activities related to our physical and mental health are reported, adding more uses to the traditional ones. At present, essential oils find applications in the sanitary, cosmetic, pharmaceutical, food, and agricultural industries, with research underway aiming at new targets and innovative ways to use them. This includes their use as feed additives in ruminants to reduce methane emanating from food digestion, or as green pesticides in the form of nano-capsules or nano-emulsions.

The hugely diverse biological activity of essential (or volatile) oils is due to their composition. They are mixtures of low-molecular-weight compounds, belonging primarily (but not exclusively) to the chemical family of terpenoids. More than a hundred such compounds may be present in an essential oil, with concentrations varying from trace to higher than 70%. These compounds may behave in additive, synergistic, or antagonistic ways, producing unique effects depending on the target organisms. Research so far with microbes shows that essential oils interact with cell membranes. Round-shaped and Gram-negative bacteria are generally less sensitive to essential oils than rod-shaped and Gram-positive ones, with the hydrophilic or lipophilic properties of essential oil constituents playing a role in the produced effect, and with oxygenated compounds being more active than hydrocarbons as growth inhibitors.

Because of their volatile nature, essential oils emanate in the environment, playing their role in chemical communication and offering resistance against both biotic and abiotic stresses. In the atmosphere, they participate as VOCs (volatile organic compounds) in the formation of air pollutants. It is estimated that chemical degradation is by far the largest sink of VOCs, with deposition having only a minor contribution. Nevertheless, soil and soil dwellers are primary recipients of these secondary metabolites, as plants do not economize in them once they are produced; plants’ dead parts contain large amounts of them. Once in soil, essential oil constituents influence soil communities and soil processes, as they are or after they are transformed chemically or biologically. Succession, litter decomposition, nutrient cycling, and enzymatic activity are among the processes that can be affected, as well as degrading microbes and other communities of the detritus food chain and mycorrhizal fungi. Given our very limited knowledge on soil responses in the presence of essential oils and their impacts on ecosystem functioning, contributions in this area are valuable—particularly if they provide some insight into responses and impacts at different scales and under different environmental regimes.

Aromatic plants are abundant in the fragrant Mediterranean environment, but essential-oil-producing plants also occur in cold climates, so that an understanding of how these secondary metabolites influence processes and communities is of global interest. This interest is further enhanced given the current re-evaluation of the methods and practices of agriculture. The paradigm shift towards sustainable farming asks for inputs like eco-friendly, target-specific, and biodegradable pesticides that do not undermine the ecosystem services. The naturally derived and fully biodegradable essential oils which influence a large spectrum of organisms in various ways are serious candidates as green pesticides, and a great deal of research is currently underway in this area.

Given the ever-increasing interest in aromatic plants and essential oils, as well as the importance of these secondary metabolites, a Special Issue is being prepared in Plants dedicated to their interplay with microbes. We welcome contributions on all sorts of interactions between essential-oil-producing plants and microbes of any kind, on interactions between aromatic plants and other organisms that are mediated by microbes, on effects involving microbes that may be attributed to essential oils or their constituents, on related processes and mechanisms, on impacts that may be direct or indirect, and on applications that they may find, focusing on the natural and agricultural environments. Original contributions will be given priority over review articles. The deadline for manuscript submission is 28 February 2022.

Prof. Dr. Despina Vokou
Guest Editor

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Keywords

  • aromatic plants
  • biological activity
  • essential oils
  • decomposition
  • green pesticides
  • phyllosphere
  • plant–microbe interactions
  • soil metabolism
  • microbial communities
  • terpenoids

Published Papers (6 papers)

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Research

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13 pages, 3323 KiB  
Article
Cinnamaldehyde Loaded Poly(lactide-co-glycolide) (PLGA) Microparticles for Antifungal Delivery Application against Resistant Candida albicans and Candida glabrata
by Silvia Rizzo, Maura Di Vito, Elena Mazzinelli, Ilaria Favuzzi, Riccardo Torelli, Margherita Cacaci, Alessandro Arcovito, Maurizio Sanguinetti, Stefania Garzoli, Giuseppina Nocca and Francesca Bugli
Plants 2023, 12(13), 2437; https://doi.org/10.3390/plants12132437 - 24 Jun 2023
Cited by 2 | Viewed by 1197
Abstract
Researchers have explored natural products to combat the antibiotic resistance of various microorganisms. Cinnamaldehyde (CIN), a major component of cinnamon essential oil (CC-EO), has been found to effectively inhibit the growth of bacteria, fungi, and mildew, as well as their production of toxins. [...] Read more.
Researchers have explored natural products to combat the antibiotic resistance of various microorganisms. Cinnamaldehyde (CIN), a major component of cinnamon essential oil (CC-EO), has been found to effectively inhibit the growth of bacteria, fungi, and mildew, as well as their production of toxins. Therefore, this study aimed to create a delivery system for CIN using PLGA microparticles (CIN-MPs), and to compare the antifungal activity of the carried and free CIN, particularly against antibiotic-resistant strains of Candida spp. The first part of the study focused on synthesizing and characterizing the PLGA MPs, which had no toxic effects in vivo and produced results in line with the existing literature. The subsequent experiments analyzed the antifungal effects of MPs-CIN on Candida albicans and Candida glabrata, both resistant (R) and sensitive (S) strains and compared its efficacy with the conventional addition of free CIN to the culture medium. The results indicated that conveyed CIN increased the antifungal effects of the product, particularly towards C. albicans R. The slow and prolonged release of CIN from the PLGA MPs ensured a constant and uniform concentration of the active principle within the cells. Full article
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22 pages, 2667 KiB  
Article
Synergistic Activity of Thymol with Commercial Antibiotics against Critical and High WHO Priority Pathogenic Bacteria
by Cristina Gan, Elisa Langa, Antonio Valenzuela, Diego Ballestero and M. Rosa Pino-Otín
Plants 2023, 12(9), 1868; https://doi.org/10.3390/plants12091868 - 2 May 2023
Cited by 7 | Viewed by 3127
Abstract
The use of synergistic combinations between natural compounds and commercial antibiotics may be a good strategy to fight against microbial resistance, with fewer side effects on human, animal and environmental, health. The antimicrobial capacity of four compounds of plant origin (thymol and gallic, [...] Read more.
The use of synergistic combinations between natural compounds and commercial antibiotics may be a good strategy to fight against microbial resistance, with fewer side effects on human, animal and environmental, health. The antimicrobial capacity of four compounds of plant origin (thymol and gallic, salicylic and gentisic acids) was analysed against 14 pathogenic bacteria. Thymol showed the best antimicrobial activity, with MICs ranging from 125 µg/mL (for Acinetobacter baumannii, Pasteurella aerogenes, and Salmonella typhimurium) to 250 µg/mL (for Bacillus subtilis, Klebsiella aerogenes, Klebsiella pneumoniae, Serratia marcescens, Staphylococcus aureus, and Streptococcus agalactiae). Combinations of thymol with eight widely used antibiotics were studied to identify combinations with synergistic effects. Thymol showed synergistic activity with chloramphenicol against A. baumannii (critical priority by the WHO), with streptomycin and gentamicin against Staphylococcus aureus (high priority by the WHO), and with streptomycin against Streptococcus agalactiae, decreasing the MICs of these antibiotics by 75% to 87.5%. The kinetics of these synergies indicated that thymol alone at the synergy concentration had almost no effect on the maximum achievable population density and very little effect on the growth rate. However, in combination with antibiotics at the same concentration, it completely inhibited growth, confirming its role in facilitating the action of the antibiotic. The time–kill curves indicated that all the combinations with synergistic effects were mainly bactericidal. Full article
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13 pages, 1228 KiB  
Article
Maltodextrin-Coated Peppermint and Caraway Essential Oils Effects on Soil Microbiota
by Maria Chmiel, Gabriela Drzymała, Jan Bocianowski, Andreja Komnenić, Agnieszka Baran and Agnieszka Synowiec
Plants 2022, 11(23), 3343; https://doi.org/10.3390/plants11233343 - 2 Dec 2022
Cited by 1 | Viewed by 1612
Abstract
Essential oils exhibit strong antimicrobial effects that can serve as a substitute for synthetic pesticides. However, many reports mention the use of essential oils in protecting above-ground plant organs and storing raw materials and seeds, but only a few address the effects of [...] Read more.
Essential oils exhibit strong antimicrobial effects that can serve as a substitute for synthetic pesticides. However, many reports mention the use of essential oils in protecting above-ground plant organs and storing raw materials and seeds, but only a few address the effects of treatments on soil microbiota. Regarding this, it is necessary to find a solution that will prevent the rapid degradation of oils in soil and extend the period of their action on the soil microbiota. The solution to this problem can be microencapsulation, where the choice of carrier plays a key role. In our experiment, maltodextrin was studied, often used in the microencapsulation of essential oils. It was examined independently in two doses (M1 and M2, with 50 and 200 g kg−1, respectively) and a combination with two essential oils known for their antimicrobial activity. We hypothesized that the selected microbial communities would react differently to the stress caused by maltodextrin-encapsulated essential oils. The serial dilution method assessed the number of colony-forming units (CFU) of bacteria, fungi, and actinomycetes. As the goal of microencapsulation was to prolong the effect of essential oils, their reaction was observed over a longer period. The soil microbial populations were examined in sandy and loamy soil at 1, 7, 14, and 78 days after encapsulated essential oils were mixed with the soil samples. In both types of soil, a significant increase in bacteria and actinomycetes was observed with maltodextrin in both doses. Encapsulated peppermint and caraway oils had different effects on microbes, both inhibitory and stimulatory. It is also important to note that peppermint with a smaller dose of maltodextrin significantly inhibited the growth of fungi in sandy soil in all measurements, as well as that caraway oil with a higher dose of maltodextrin significantly stimulated the growth of bacteria and actinomycetes in sandy soil. The higher dose of maltodextrin could explain this stimulation. Further research is recommended to test different doses of essential oils and maltodextrin, which would lead to the optimal dose of both wall and core materials. Full article
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19 pages, 2724 KiB  
Article
Monoterpene Enrichments Have Positive Impacts on Soil Bacterial Communities and the Potential of Application in Bioremediation
by Dimitris Chalkos, Katerina Karamanoli and Despoina Vokou
Plants 2021, 10(11), 2536; https://doi.org/10.3390/plants10112536 - 21 Nov 2021
Cited by 7 | Viewed by 1721
Abstract
We study here how soil bacterial communities of different ecosystems respond to disturbances caused by enrichments with monoterpenes that are common essential oil constituents. We used fenchone, 1,8-cineol and α-pinene, and soils from phrygana, a typical Mediterranean-type ecosystem where aromatic plants abound, and [...] Read more.
We study here how soil bacterial communities of different ecosystems respond to disturbances caused by enrichments with monoterpenes that are common essential oil constituents. We used fenchone, 1,8-cineol and α-pinene, and soils from phrygana, a typical Mediterranean-type ecosystem where aromatic plants abound, and from another five ecosystem types, focusing on culturable bacteria. Patterns of response were common to all ecosystems, but responses themselves were not always as pronounced in phrygana as in the other ecosystems, suggesting that these enrichments are less of a disturbance there. More specifically, soil respiration and abundance of the bacterial communities increased, becoming from below two up to 16 times as high as in control soils (for both attributes) and remained at high levels as long as these compounds were present. Bacteria that can utilize these three compounds as substrates of growth became dominant members of the bacterial communities in the enriched soils. All changes were readily reversible once monoterpene addition stopped. Bacteria with the ability to utilize these monoterpenes as carbon sources were found in soils from all ecosystems, 15 strains in total, suggesting a rather universal presence; of these, six could also utilize the organic pollutants toluene or p-xylene. These results suggest also potential novel applications of monoterpenes in combating soil pollution. Full article
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19 pages, 4184 KiB  
Article
Impacts of Decaying Aromatic Plants on the Soil Microbial Community and on Tomato Seedling Growth and Metabolism: Suppression or Stimulation?
by Aggeliki Ainalidou, Foteini Bouzoukla, Urania Menkissoglu-Spiroudi, Despoina Vokou and Katerina Karamanoli
Plants 2021, 10(9), 1848; https://doi.org/10.3390/plants10091848 - 6 Sep 2021
Cited by 6 | Viewed by 2155
Abstract
This study provides insight into changes in the features of tomato seedlings growing in soils enriched with spearmint, peppermint, or rosemary leaves and into changes in the microbial communities of these soils used as seedbeds; an organic amendment was also applied as a [...] Read more.
This study provides insight into changes in the features of tomato seedlings growing in soils enriched with spearmint, peppermint, or rosemary leaves and into changes in the microbial communities of these soils used as seedbeds; an organic amendment was also applied as a positive control. While the soil microbial community flourished in the presence of all three aromatic plants, tomato growth was inhibited or stimulated depending on the plant that was used. More specifically, phospholipid fatty acid (PLFA) analysis showed an increase in the total microbial biomass and in the biomass of all the groups examined, except for actinobacteria, and changes in the microbial community structure, with Gram-negative bacteria and fungi being favoured in the mint treatments, in which the microbial biomass was maximized. Seedlings from the rosemary treatment were entirely inhibited; they were at the open-cotyledon stage throughout the experiment. Seedlings from the mint treatments were the heaviest, longest, and had the highest chlorophyll content and photosynthetic yield. Metabolomic analysis showed metabolism enhancement associated with both growth and priming in seedlings from the mint treatments and disruption of metabolic pathways in those from the rosemary treatment. There is a great potential for applying these aromatic plants as soil amendments and as either biostimulants of plant growth or as herbicides. Full article
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Review

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26 pages, 1770 KiB  
Review
Biocontrol Activity of Aromatic and Medicinal Plants and Their Bioactive Components against Soil-Borne Pathogens
by Babett Greff, András Sáhó, Erika Lakatos and László Varga
Plants 2023, 12(4), 706; https://doi.org/10.3390/plants12040706 - 5 Feb 2023
Cited by 20 | Viewed by 4569
Abstract
Soil-borne phytopathogens can have detrimental effects on both cereal and horticultural crops resulting in serious losses worldwide. Due to their high efficiency and easy applicability, synthetic pesticides are still the primary choice in modern plant disease control systems, but stringent regulations and increasing [...] Read more.
Soil-borne phytopathogens can have detrimental effects on both cereal and horticultural crops resulting in serious losses worldwide. Due to their high efficiency and easy applicability, synthetic pesticides are still the primary choice in modern plant disease control systems, but stringent regulations and increasing environmental concerns make the search for sustainable alternatives more pressing than ever. In addition to the incorporation of botanicals into agricultural practices, the diversification of cropping systems with aromatic and medicinal plants is also an effective tool to control plant diseases through providing nutrients and shaping soil microbial communities. However, these techniques are not universally accepted and may negatively affect soil fertility if their application is not thoroughly controlled. Because the biocontrol potential of aromatic and medicinal plants has been extensively examined over the past decades, the present study aims to overview the recent literature concerning the biopesticide effect of secondary metabolites derived from aromatic and medicinal plants on important soil-borne plant pathogens including bacteria, fungi, and nematodes. Most of the investigated herbs belong to the family of Lamiaceae (e.g., Origanum spp., Salvia spp., Thymus spp., Mentha spp., etc.) and have been associated with potent antimicrobial activity, primarily due to their chemical constituents. The most frequently tested organisms include fungi, such as Rhizoctonia spp., Fusarium spp., and Phytophthora spp., which may be highly persistent in soil. Despite the intense research efforts dedicated to the development of plant-based pesticides, only a few species of aromatic herbs are utilized for the production of commercial formulations due to inconsistent efficiency, lack of field verification, costs, and prolonged authorization requirements. However, recycling the wastes from aromatic and medicinal plant-utilizing industries may offer an economically feasible way to improve soil health and reduce environmental burdens at the same time. Overall, this review provides comprehensive knowledge on the efficiency of aromatic herb-based plant protection techniques, and it also highlights the importance of exploiting the residues generated by aromatic plant-utilizing sectors as part of agro-industrial processes. Full article
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