Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Microbial volatile organic compounds in intra-kingdom and inter-kingdom interactions

Nature Reviews Microbiology volume 19, pages 391–404 (2021)Cite this article

Subjects

Abstract

Microorganisms produce and excrete a versatile array of metabolites with different physico-chemical properties and biological activities. However, the ability of microorganisms to release volatile compounds has only attracted research attention in the past decade. Recent research has revealed that microbial volatiles are chemically very diverse and have important roles in distant interactions and communication. Microbial volatiles can diffuse fast in both gas and water phases, and thus can mediate swift chemical interactions. As well as constitutively emitted volatiles, microorganisms can emit induced volatiles that are triggered by biological interactions or environmental cues. In this Review, we highlight recent discoveries concerning microbial volatile compounds and their roles in intra-kingdom microbial interactions and inter-kingdom interactions with plants and insects. Furthermore, we indicate the potential biotechnological applications of microbial volatiles and discuss challenges and perspectives in this emerging research field.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Volatile derivatives of primary metabolism.
Fig. 2: Volatile aromatic compounds and sulfur-containing compounds.
Fig. 3: Volatile formation via the fatty acid biosynthetic pathway.
Fig. 4: Biosynthesis of volatile terpenes.
Fig. 5: Major biosynthetic pathways of microbial volatile organic compounds.
Fig. 6: Modes of diffusion of microbial volatiles and responses in microorganisms, plants and animals to their exposure.

Similar content being viewed by others

References

  1. Whiteley, M., Diggle, S. P. & Greenberg, E. P. Progress in and promise of bacterial quorum sensing research. Nature 551, 313–320 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Papenfort, K. & Bassler, B. L. Quorum sensing signal-response systems in Gram-negative bacteria. Nat. Rev. Microbiol. 14, 576–588 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Schulz, S. & Dickschat, J. S. Bacterial volatiles: the smell of small organisms. Nat. Prod. Rep. 24, 814–842 (2007). This work is the first to bring research attention to the importance of microbial volatiles.

    CAS  PubMed  Google Scholar 

  4. Farag, M. A. et al. Biological and chemical strategies for exploring inter- and intra-kingdom communication mediated via bacterial volatile signals. Nat. Protoc. 12, 1359–1377 (2017). This work provides an overview of in vitro methods for evaluating bacterial and plant responses to bacterial volatile compounds.

    CAS  PubMed  Google Scholar 

  5. Schulz-Bohm, K., Martin-Sanchez, L. & Garbeva, P. Microbial volatiles: small molecules with an important role in intra- and inter-kingdom interactions. Front. Microbiol. 8, https://doi.org/10.3389/fmicb.2017.02484 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Boland, W. The chemistry of gamete attraction — chemical structures, biosynthesis, and (a)biotic degradation of algal pheromones. Proc. Natl Acad. Sci. USA 92, 37–43 (1995).

    CAS  PubMed  Google Scholar 

  7. Pappas, C., Tzakos, A. G. & Gerothanassis, I. P. On the hydration state of amino acids and their derivatives at different ionization states: a comparative multinuclear NMR and crystallographic investigation. J. Peptide Sci. 18, S165–S165 (2012).

    Google Scholar 

  8. Dickschat, J. S. et al. Pyrazine biosynthesis in Corynebacterium glutamicum. Eur. J. Org. Chem. 14, 2687–2695 (2010).

    Google Scholar 

  9. Nawrath, T., Dickschat, J. S., Kunze, B. & Schulz, S. The biosynthesis of branched dialkylpyrazines in myxobacteria. Chem. Biodivers. 7, 2129–2144 (2010).

    CAS  PubMed  Google Scholar 

  10. Kretsch, A. M. et al. Discovery of (dihydro)pyrazine N-oxides via genome mining in Pseudomonas. Org. Lett. 20, 4791–4795 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Beck, H. C., Hansen, A. M. & Lauritsen, F. R. Novel pyrazine metabolites found in polymyxin biosynthesis by Paenibacillus polymyxa. FEMS Microbiol. Lett. 220, 67–73 (2003).

    CAS  PubMed  Google Scholar 

  12. Dickschat, J. S., Reichenbach, H., Wagner-Dobler, I. & Schulz, S. Novel pyrazines from the myxobacterium Chondromyces crocatus and marine bacteria. Eur. J. Org. Chem. https://doi.org/10.1002/ejoc.200500280 (2005).

    Article  Google Scholar 

  13. Brock, N. L., Menke, M., Klapschinski, T. A. & Dickschat, J. S. Marine bacteria from the Roseobacter clade produce sulfur volatiles via amino acid and dimethylsulfoniopropionate catabolism. Org. Biomol. Chem. 12, 4318–4323 (2014).

    CAS  PubMed  Google Scholar 

  14. Bentley, R. & Chasteen, T. G. Environmental VOSCs — formation and degradation of dimethyl sulfide, methanethiol and related materials. Chemosphere 55, 291–317 (2004).

    CAS  PubMed  Google Scholar 

  15. Dickschat, J. S., Wenzel, S. C., Bode, H. B., Muller, R. & Schulz, S. Biosynthesis of volatiles by the myxobacterium Myxococcus xanthus. ChemBioChem 5, 778–787 (2004).

    CAS  PubMed  Google Scholar 

  16. Yamada, Y. et al. Terpene synthases are widely distributed in bacteria. Proc. Natl Acad. Sci. USA 112, 857–862 (2015).

    CAS  PubMed  Google Scholar 

  17. Dickschat, J. S. Bacterial terpene cyclases. Nat. Product. Rep. 33, 87–110 (2016).

    CAS  Google Scholar 

  18. Citron, C. A. & Dickschat, J. S. Microbial terpenes: a perspective on their chemistry and biosynthesis. Synlett 25, 766–782 (2014).

    CAS  Google Scholar 

  19. Schmidt, R. et al. Deciphering the genome and secondary metabolome of the plant pathogen Fusarium culmorum. FEMS Microbiol. Ecol. 94 (2018).

  20. Dickschat, J. S. Fungal volatiles — a survey from edible mushrooms to moulds. Nat. Product. Rep. 34, 310–328 (2017).

    CAS  Google Scholar 

  21. Rinkel, J., Koellner, T. G., Chen, F. & Dickschat, J. S. Characterisation of three terpene synthases for β-barbatene, β-araneosene and nephthenol from social amoebae. Chem. Commun. 55, 13255–13258 (2019).

    CAS  Google Scholar 

  22. Gurtler, H. et al. Albaflavenone, a sesquiterpene ketone with a zizaene skeleton produced by a streptomycete with a new rope morphology. J. Antibiotics 47, 434–439 (1994).

    CAS  Google Scholar 

  23. Schifrin, A. et al. A single terpene synthase is responsible for a wide variety of sesquiterpenes in Sorangium cellulosum Soce56. Org. Biomol. Chem. 14, 3385–3393 (2016).

    CAS  PubMed  Google Scholar 

  24. Brock, N. L., Ravella, S. R., Schulz, S. & Dickschat, J. S. A detailed view of 2-methylisoborneol biosynthesis. Angew. Chem. Int. Ed. 52, 2100–2104 (2013).

    CAS  Google Scholar 

  25. Jiang, J., He, X. & Cane, D. E. Biosynthesis of the earthy odorant geosmin by a bifunctional Streptomyces coelicolor enzyme. Nat. Chem. Biol. 3, 711–715 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. von Reuss, S. et al. Sodorifen biosynthesis in the rhizobacterium Serratia plymuthica involves methylation and cyclization of MEP-derived farnesyl pyrophosphate by a SAM-dependent C-methyltransferase. J. Am. Chem. Soc. 140, 11855–11862 (2018).

    Google Scholar 

  27. Lee, J.-H., Wood, T. K. & Lee, J. Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol. 23, 707–718 (2015).

    CAS  PubMed  Google Scholar 

  28. Martin-Sanchezt, L. et al. Phylogenomic analyses and distribution of terpene synthases among Streptomyces. Beilstein J. Org. Chem. 15, 1181–1193 (2019).

    Google Scholar 

  29. Blom, D. et al. Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ. Microbiol. 13, 3047–3058 (2011).

    CAS  PubMed  Google Scholar 

  30. Groenhagen, U., Maczka, M., Dickschat, J. S. & Schulz, S. Streptopyridines, volatile pyridine alkaloids produced by Streptomyces sp. FORM5. Beilstein J. Org. Chem. 10, 1421–1432 (2014).

    PubMed  PubMed Central  Google Scholar 

  31. Groenhagen, U., De Oliveira, A. L. L., Fielding, E., Moore, B. S. & Schulz, S. Coupled biosynthesis of volatiles and aalinosporamide A in Salinispora tropica. ChemBioChem 17, 1978–1985 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Schlawis, C. et al. Structural elucidation of trace components combining GC/MS, GC/IR, DFT-calculation and synthesis — salinilactones, unprecedented bicyclic lactones from Salinispora bacteria. Angew. Chem. Int. Ed. 57, 14921–14925 (2018).

    CAS  Google Scholar 

  33. Schmidt, R. et al. Fungal volatile compounds induce production of the secondary metabolite sodorifen in Serratia plymuthica PRI-2C. Sci. Rep. 7, 862 (2017).

    PubMed  PubMed Central  Google Scholar 

  34. van Dam, N. M., Weinhold, A., & Garbeva, P. Calling in the Dark: The Role of Volatiles for Communication in the Rhizosphere 175–210 (Springer, 2016).

  35. Garbeva, P., Hordijk, C., Gerards, S. & de Boer, W. Volatiles produced by the mycophagous soil bacterium Collimonas. FEMS Microbiol. Ecol. 87, 639–649 (2014).

    CAS  PubMed  Google Scholar 

  36. Lazazzara, V. et al. Growth media affect the volatilome and antimicrobial activity against Phytophthora infestans in four Lysobacter type strains. Microbiol. Res. 201, 52–62 (2017).

    CAS  PubMed  Google Scholar 

  37. Schulz, S., Fuhlendorff, J. & Reichenbach, H. Identification and synthesis of volatiles released by the myxobacterium Chondromyces crocatus. Tetrahedron 60, 3863–3872 (2004).

    CAS  Google Scholar 

  38. Schmidt, R. et al. Microbial small talk: volatiles in fungal–bacterial interactions. Front. Microbiol. https://doi.org/10.3389/fmicb.2015.01495 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Kai, M. et al. Serratia odorifera: analysis of volatile emission and biological impact of volatile compounds on Arabidopsis thaliana. Appl. Microbiol. Biotechnol. 88, 965–976 (2010).

    CAS  PubMed  Google Scholar 

  40. Chen, X. et al. Diversity and functional evolution of terpene synthases in dictyostelid social amoebae. Sci. Rep. https://doi.org/10.1038/s41598-018-32639-0 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Tyc, O., Zweers, H., de Boer, W. & Garbeva, P. Volatiles in inter-specific bacterial interactions. Front. Microbiol. 6 (2015).

  42. Schulz-Bohm, K., Zweers, H., de Boer, W. & Garbeva, P. A fragrant neighborhood: volatile mediated bacterial interactions in soil. Front. Microbiol. 6 (2015).

  43. Abis, L. et al. Reduced microbial diversity induces larger volatile organic compound emissions from soils. Sci. Rep. 10, 6104–6104 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. van Agtmaal, M. et al. Legacy effects of anaerobic soil disinfestation on soil bacterial community composition and production of pathogen-suppressing volatiles. Front. Microbiol. https://doi.org/10.3389/fmicb.2015.00701 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Hol, W. H. G. et al. Non-random species loss in bacterial communities reduces antifungal volatile production. Ecology 96, 2042–2048 (2015).

    PubMed  Google Scholar 

  46. Carrion, V. J. et al. Involvement of Burkholderiaceae and sulfurous volatiles in disease-suppressive soils. ISME J. 12, 2307–2321 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Cordovez, V. et al. Diversity and functions of volatile organic compounds produced by Streptomyces from a disease-suppressive soil. Front. Microbiol. https://doi.org/10.5589/fmicb.2015.01081 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  48. Ossowicki, A. et al. Microbial and volatile profiling of soils suppressive to Fusarium culmorum of wheat. Proc. Biol. Sci. 287, 20192527 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Audrain, B., Farag, M. A., Ryu, C.-M. & Ghigo, J.-M. Role of bacterial volatile compounds in bacterial biology. FEMS Microbiol. Rev. 39, 222–233 (2015).

    CAS  PubMed  Google Scholar 

  50. Schmidt, R., Cordovez, V., de Boer, W., Raaijmakers, J. & Garbeva, P. Volatile affairs in microbial interactions. ISME J. 9, 2329–2335 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Avalos, M., van Wezell, G. P., Raaijmakers, J. M. & Garbeva, P. Healthy scents: microbial volatiles as new frontier in antibiotic research? Curr. Opin. Microbiol. 45, 84–91 (2018).

    CAS  PubMed  Google Scholar 

  52. Kim, K.-s., Lee, S. & Ryu, C.-M. Interspecific bacterial sensing through airborne signals modulates locomotion and drug resistance. Nat. Commun. https://doi.org/10.1038/ncomms2789 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Briard, B., Heddergott, C. & Latge, J.-P. Volatile compounds emitted by Pseudomonas aeruginosa stimulate growth of the fungal pathogen Aspergillus fumigatus. Mbio https://doi.org/10.1128/mBio.00219-16 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Letoffe, S., Audrain, B., Bernier, S. P., Delepierre, M. & Ghigo, J.-M. Aerial exposure to the bacterial volatile compound trimethylamine modifies antibiotic resistance of physically separated bacteria by raising culture medium pH. Mbio https://doi.org/10.1128/mBio.00944-13 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Chen, Y., Gozzi, K., Yan, F. & Chai, Y. Acetic acid acts as a volatile signal to stimulate bacterial biofilm formation. Mbio https://doi.org/10.1128/mBio.00392-15 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Garbeva, P., Hordijk, C., Gerards, S. & De Boer, W. Volatile-mediated interactions between phylogenetically different soil bacteria. Front. Microbiol. https://doi.org/10.3389/fmicb.2014.00289 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Meldau, D. G. et al. Dimethyl disulfide produced by the naturally associated bacterium Bacillus sp B55 promotes Nicotiana attenuata growth by enhancing sulfur nutrition. Plant Cell 25, 2731–2747 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Jones, S. E. et al. Streptomyces exploration is triggered by fungal interactions and volatile signals. eLife https://doi.org/10.7554/eLife.21738 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Rybakova, D. et al. Aerial warfare: a volatile dialogue between the plant pathogen Verticillium longisporum and its antagonist Paenibacillus polymyxa. Front. Plant Sci. 8 (2017).

  60. Spraker, J. E. et al. A volatile relationship: profiling an inter-kingdom dialogue between two plant pathogens, Ralstonia solanacearum and Aspergillus flavus. J. Chem. Ecol. 40, 502–513 (2014).

    CAS  PubMed  Google Scholar 

  61. Tyagi, S., Lee, K.-J., Shukla, P. & Chae, J.-C. Dimethyl disulfide exerts antifungal activity against Sclerotinia minor by damaging its membrane and induces systemic resistance in host plants. Sci. Rep. 10, 6547–6547 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Alpha, C. J., Campos, M., Jacobs-Wagner, C. & Strobela, S. A. Mycofumigation by the volatile organic compound-producing fungus Muscodor albus induces bacterial cell death through DNA damage. Appl. Environ. Microbiol. 81, 1147–1156 (2015).

    PubMed  PubMed Central  Google Scholar 

  63. Trombetta, D. et al. Mechanisms of antibacterial action of three monoterpenes. Antimicrob. Agents Chemother. 49, 2474–2478 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Schulz-Bohm, K. et al. The prey’s scent — volatile organic compound mediated interactions between soil bacteria and their protist predators. ISME J. 11, 817–820 (2017). This work demonstrates for the first time that volatiles are directly involved in protist−bacterial predator−prey interactions.

    CAS  PubMed  Google Scholar 

  65. Ryu, C. M. et al. Bacterial volatiles promote growth in Arabidopsis. Proc. Natl Acad. Sci. USA 100, 4927–4932 (2003). This study is the first to reveal that bacterial volatiles can promote plant growth.

    CAS  PubMed  Google Scholar 

  66. Maria Sanchez-Lopez, A. et al. Volatile compounds emitted by diverse phytopathogenic microorganisms promote plant growth and flowering through cytokinin action. Plant Cell Environ. 39, 2592–2608 (2016).

    Google Scholar 

  67. Velazquez-Becerra, C. et al. A volatile organic compound analysis from Arthrobacter agilis identifies dimethylhexadecylamine, an amino-containing lipid modulating bacterial growth and Medicago sativa morphogenesis in vitro. Plant Soil 339, 329–340 (2011).

    CAS  Google Scholar 

  68. Wenke, K. et al. Volatiles of two growth-inhibiting rhizobacteria commonly engage AtWRKY18 function. Plant J. 70, 445–459 (2012).

    CAS  PubMed  Google Scholar 

  69. Ulloa-Benitez, A. et al. Phytotoxic and antimicrobial activity of volatile and semi-volatile organic compounds from the endophyte Hypoxylon anthochroum strain Blaci isolated from Bursera lancifolia (Burseraceae). J. Appl. Microbiol. 121, 380–400 (2016).

    CAS  PubMed  Google Scholar 

  70. Kai, M. & Piechulla, B. Plant growth promotion due to rhizobacterial volatiles — an effect of CO2? FEBS Lett. 583, 3473–3477 (2009).

    CAS  PubMed  Google Scholar 

  71. Groenhagen, U. et al. Production of bioactive volatiles by different Burkholderia ambifaria strains. J. Chem. Ecol. 39, 892–906 (2013).

    CAS  PubMed  Google Scholar 

  72. Bailly, A. et al. The inter-kingdom volatile signal indole promotes root development by interfering with auxin signalling. Plant J. 80, 758–771 (2014). This study reveals that indole, beyond its importance as a bacterial signal molecule, can serve as a remote messenger to manipulate plant growth and development.

    CAS  PubMed  Google Scholar 

  73. Zhang, H. et al. Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226, 839–851 (2007).

    CAS  PubMed  Google Scholar 

  74. Kwon, Y. S. et al. Proteome analysis of Arabidopsis seedlings exposed to bacterial volatiles. Planta 232, 1355–1370 (2010).

    CAS  PubMed  Google Scholar 

  75. Zhang, H. et al. Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J. 56, 264–273 (2008).

    CAS  PubMed  Google Scholar 

  76. Zhang, H. et al. A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J. 58, 568–577 (2009).

    CAS  PubMed  Google Scholar 

  77. del Carmen Orozco-Mosqueda, M., Macias-Rodriguez, L. I., Santoyo, G., Farias-Rodriguez, R. & Valencia-Cantero, E. Medicago truncatula increases its iron-uptake mechanisms in response to volatile organic compounds produced by Sinorhizobium meliloti. Folia Microbiol. 58, 579–585 (2013).

    Google Scholar 

  78. Garbeva, P. & Weisskopf, L. Airborne medicine: bacterial volatiles and their influence on plant health. New Phytol. 226, 32–43 (2019).

    PubMed  Google Scholar 

  79. Pieterse, C. M. J. et al. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52, 347–375 (2014).

    CAS  PubMed  Google Scholar 

  80. Ryu, C. M. et al. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134, 1017–1026 (2004). This study provides new insight into the role of bacteria volatile organic compounds as initiators of defence responses in plants.

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Han, S. H. et al. GacS-dependent production of 2R,3R-butanediol by Pseudomonas chlororaphis O6 is a major determinant for eliciting systemic resistance against Erwinia carotovora but not against Pseudomonas syringae pv. tabaci in tobacco. Mol. Plant Microbe Interact. 19, 924–930 (2006).

    CAS  PubMed  Google Scholar 

  82. Song, G. C. et al. Plant growth-promoting archaea trigger induced systemic resistance in Arabidopsis thaliana against Pectobacterium carotovorum and Pseudomonas syringae. Environ. Microbiol. 21, 940–948 (2019).

    CAS  PubMed  Google Scholar 

  83. Zhang, H. et al. Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol. Plant Microbe Interact. 21, 737–744 (2008).

    PubMed  Google Scholar 

  84. Ledger, T. et al. Volatile-mediated effects predominate in Paraburkholderia phytofirmans growth promotion and salt stress tolerance of Arabidopsis thaliana. Front. Microbiol. 7, 1838 (2016).

    PubMed  PubMed Central  Google Scholar 

  85. Cho, S. M. et al. 2R,3R-Butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol. Plant Microbe Interact. 21, 1067–1075 (2008).

    CAS  PubMed  Google Scholar 

  86. Vaishnav, A., Kumari, S., Jain, S., Varma, A. & Choudhary, D. K. Putative bacterial volatile-mediated growth in soybean (Glycine max L. Merrill) and expression of induced proteins under salt stress. J. Appl. Microbiol. 119, 539–551 (2015).

    CAS  PubMed  Google Scholar 

  87. Bhattacharyya, D., Yu, S.-M. & Lee, Y. H. Volatile compounds from Alcaligenes faecalis JBCS1294 confer salt tolerance in Arabidopsis thaliana through the auxin and gibberellin pathways and differential modulation of gene expression in root and shoot tissues. Plant Growth Regul. 75, 297–306 (2015).

    CAS  Google Scholar 

  88. Zhang, H. et al. Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol. Plant Microbe Interact. 23, 1097–1104 (2010).

    CAS  PubMed  Google Scholar 

  89. Ditengou, F. A. et al. Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture. Nat. Commun. https://doi.org/10.1038/ncomms7279 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Bitas V., McCartney N., Li N., Demers J., Kim J-E, Kim H-S, Brown K.M. and Kang S. Fusarium oxysporum volatiles enhance plant growth via affecting auxin transport and signaling. Front. Microbiol. 6, 1248 (2015).

    PubMed  PubMed Central  Google Scholar 

  91. Li, N. et al. Volatile compounds emitted by diverse Verticillium species enhance plant growth by manipulating auxin signaling. Mol. Plant Microbe Interact. 31, 1021–1031 (2018).

    CAS  PubMed  Google Scholar 

  92. Moisan, K. et al. Volatiles of pathogenic and non-pathogenic soil-borne fungi affect plant development and resistance to insects. Oecologia 190, 589–604 (2019).

    PubMed  PubMed Central  Google Scholar 

  93. Erb, M. et al. Indole is an essential herbivore-induced volatile priming signal in maize. Nat. Commun. 6, 6273 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Kremr, D. et al. Using headspace solid-phase microextraction for comparison of volatile sulphur compounds of fresh plants belonging to families Alliaceae and Brassicaceae. J. Food Sci. Technol. 52, 5727–5735 (2015).

    CAS  PubMed  Google Scholar 

  95. Robacker, D. C. & Lauzon, C. R. Purine metabolizing capability of Enterobacter agglomerans affects volatiles production and attractiveness to Mexican fruit fly. J. Chem. Ecol. 28, 1549–1563 (2002).

    CAS  PubMed  Google Scholar 

  96. Robacker, D. C., Lauzon, C. R. & He, X. D. Volatiles production and attractiveness to the Mexican fruit fly of Enterobacter agglomerans isolated from apple maggot and Mexican fruit flies. J. Chem. Ecol. 30, 1329–1347 (2004).

    CAS  PubMed  Google Scholar 

  97. Stensmyr, M. C. et al. A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151, 1345–1357 (2012).

    CAS  PubMed  Google Scholar 

  98. Melo, N. et al. Geosmin attracts Aedes aegypti mosquitoes to oviposition sites. Curr. Biol. 30, 127–134 (2020).

    CAS  PubMed  Google Scholar 

  99. Becher, P. G. et al. Developmentally regulated volatiles geosmin and 2-methylisoborneol attract a soil arthropod to Streptomyces bacteria promoting spore dispersal. Nat. Microbiol. 5, 821–829 (2020).

    CAS  PubMed  Google Scholar 

  100. Kalinova, B., Podskalska, H., Ruzicka, J. & Hoskovec, M. Irresistible bouquet of death-how are burying beetles (Coleoptera: Silphidae: Nicrophorus) attracted by carcasses. Naturwissenschaften 96, 889–899 (2009).

    CAS  PubMed  Google Scholar 

  101. Christiaens, J. F. et al. The fungal aroma gene ATF1 promotes dispersal of yeast cells through insect vectors. Cell Rep. 9, 425–432 (2014).

    CAS  PubMed  Google Scholar 

  102. Ljunggren, J. et al. Yeast volatomes differentially affect larval feeding in an insect herbivore. Appl. Environ. Microbiol. 85, e01761-19 (2019).

    PubMed  PubMed Central  Google Scholar 

  103. Ampt, E. A., Bush, D. S., Siegel, J. P. & Berenbaum, M. R. Larval preference and performance of Amyelois transitella (navel orangeworm, Lepidoptera: Pyralidae) in relation to the fungus Aspergillus flavus. Environ. Entomol. 45, 155–162 (2016).

    PubMed  Google Scholar 

  104. Zhao, T. et al. Convergent evolution of semiochemicals across kingdoms: bark beetles and their fungal symbionts. ISME J. 13, 1535–1545 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Zhu, J. J. et al. Semiochemicals released from five bacteria identified from animal wounds infested by primary screwworms and their effects on fly behavioral activity. PloS ONE 12, e0179090 (2017).

    PubMed  PubMed Central  Google Scholar 

  106. Takken, W. & Verhulst, N. O. Chemical signaling in mosquito–host interactions: the role of human skin microbiota. Curr. Opin. Insect Sci. 20, 68–74 (2017).

    PubMed  Google Scholar 

  107. Verhulst, N. O. et al. Differential attraction of malaria mosquitoes to volatile blends produced by human skin bacteria. PloS ONE 5, e15829. (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Ponnusamy, L. et al. Identification of bacteria and bacteria-associated chemical cues that mediate oviposition site preferences by Aedes aegypti. Proc. Natl Acad. Sci. USA 105, 9262–9267 (2008).

    CAS  PubMed  Google Scholar 

  109. Fischer, C. Y. et al. Bacteria may contribute to distant species recognition in ant–aphid mutualistic relationships. Insect Sci. 24, 278–284 (2017).

    CAS  PubMed  Google Scholar 

  110. Noman, A., Aqeel, M., Qasim, M., Haider, I. & Lou, Y. Plant–insect–microbe interaction: a love triangle between enemies in ecosystem. Sci. Total Environ. 699, 134181–134181 (2019).

    PubMed  Google Scholar 

  111. Rios-Covian, D. et al. Intestinal short chain fatty acids and their link with diet and human health. Front. Microbiol. 7, 185 (2016).

    PubMed  PubMed Central  Google Scholar 

  112. Louis, P., Hold, G. L. & Flint, H. J. The gut microbiota, bacterial metabolites and colorectal cancer. Nat. Rev. Microbiol. 12, 661–672 (2014).

    CAS  PubMed  Google Scholar 

  113. Smolinska, A. et al. Benefits of short-chain fatty acids and their receptors in inflammation and carcinogenesis. Anal. Chim. Acta 1025, 1–11 (2018).

    CAS  PubMed  Google Scholar 

  114. Arora, T. & Sharma, R. Fermentation potential of the gut microbiome: implications for energy homeostasis and weight management. Nutr. Rev. 69, 99–106 (2011).

    PubMed  Google Scholar 

  115. Sivaprakasam, S., Prasad, P. D. & Singh, N. Benefits of short-chain fatty acids and their receptors in inflammation and carcinogenesis. Pharmacol. Ther. 164, 144–151 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Bernier, S. P., Letoffe, S., Delepierre, M. & Ghigo, J.-M. Biogenic ammonia modifies antibiotic resistance at a distance in physically separated bacteria. Mol. Microbiol. 81, 705–716 (2011).

    CAS  PubMed  Google Scholar 

  117. Lee, H. H., Molla, M. N., Cantor, C. R. & Collins, J. J. Bacterial charity work leads to population-wide resistance. Nature 467, 82–U113 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Chernin, L. et al. Quorum-sensing quenching by rhizobacterial volatiles. Environ. Microbiol. Rep. 3, 698–704 (2011).

    CAS  PubMed  Google Scholar 

  119. Schulz, S. et al. Biological activity of volatiles from marine and terrestrial bacteria. Mar. Drugs 8, 2976–2987 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Kesarwani, M. et al. A quorum sensing regulated small volatile molecule reduces acute virulence and promotes chronic infection phenotypes. PloS Pathogens 7, e1002192 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  121. Schoeck, M., Liebminger, S., Berg, G. & Cernava, T. First evaluation of alkylpyrazine application as a novel method to decrease microbial contaminations in processed meat products. AMB Express, 8, 54 (2018).

    Google Scholar 

  122. Li, Q. et al. Biofumigation on post-harvest diseases of fruits using a new volatile-producing fungus of Ceratocystis fimbriata. PloS ONE 10, e0132009 (2015).

    PubMed  PubMed Central  Google Scholar 

  123. Wan, M., Li, G., Zhang, J., Jiang, D. & Huang, H.-C. Effect of volatile substances of Streptomyces platensis F-1 on control of plant fungal diseases. Biol. Control. 46, 552–559 (2008).

    Google Scholar 

  124. Li, Q. et al. Fumigant activity of volatiles of Streptomyces globisporus JK-1 against Penicillium italicum on Citrus microcarpa. Postharvest Biol. Technol. 58, 157–165 (2010).

    CAS  Google Scholar 

  125. Huang, R. et al. Control of postharvest botrytis fruit rot of strawberry by volatile organic compounds of Candida intermedia. Phytopathology 101, 859–869 (2011).

    CAS  PubMed  Google Scholar 

  126. Arnault, I., Fleurance, C., Vey, F., Du Fretay, G. & Auger, J. Use of Alliaceae residues to control soil-borne pathogens. Ind. Crop. Products 49, 265–272 (2013).

    CAS  Google Scholar 

  127. Pecchia, S., Franceschini, A., Santori, A., Vannacci, G. & Myrta, A. Efficacy of dimethyl disulfide (DMDS) for the control of chrysanthemum Verticillium wilt in Italy. Crop. Prot. 93, 28–32 (2017).

    CAS  Google Scholar 

  128. Mulay, P. R. et al. Acute illness associated with exposure to a new soil fumigant containing dimethyl disulfide — Hillsborough county, Florida, 2014. J. Agromedicine 21, 373–379 (2016).

    PubMed  Google Scholar 

Download references

Acknowledgements

The Netherlands Institute of Ecology (NIOO‐KNAW) publication number is 7063. Support from the Swiss National Science Foundation (grant 179310 to L.W.) and the Netherlands Science Foundation (NWO-VIDI grant 864.11.015 to P.G.) is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Department of Biology, University of Fribourg, Fribourg, Switzerland

    Laure Weisskopf

  2. Institute of Organic Chemistry, Technische Universitat Braunschweig, Braunschweig, Germany

    Stefan Schulz

  3. Netherlands Institute of Ecology (NIOO-KNAW), Department of Microbial Ecology, Wageningen, The Netherlands

    Paolina Garbeva

  4. Department of Plant and Environmental Sciences, Faculty of Natural and Life Sciences, University of Copenhagen, Copenhagen, Denmark

    Paolina Garbeva

Authors
  1. Laure Weisskopf
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefan Schulz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paolina Garbeva
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The authors contributed equally to all aspects of the article.

Corresponding author

Correspondence to Paolina Garbeva.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Microbiology thanks C. Ryu and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Glossary

Hydration sphere

The solvent or water interface of any chemical compound.

Terpene pathway

A sequence of chemical reactions in a living organism leading to the production of terpenes.

Pyrazines

A group of organic aromatic compounds having a six-member ring in which the first and fourth atoms are nitrogen atoms and the rest are carbon atoms.

Sesquiterpenes

A class of terpenes with 15 carbons that formally consist of three isoprene units, often with the molecular formula C15H24.

Damping-off disease

A horticultural disease caused by several different pathogens that kill or weaken seeds or seedlings before or after they germinate.

Olfactory cues

Signals that can be extracted from the sensory input by a perceiver, indicating the state of some property of the world that the perceiver is interested in perceiving.

DA2 glomerules

Spherical structures located in the olfactory bulb of the brain.

Electroantennography

A technique for measuring the average nerve output of an insect antenna for a given odour.

Carrion

The decaying flesh of dead animals.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Weisskopf, L., Schulz, S. & Garbeva, P. Microbial volatile organic compounds in intra-kingdom and inter-kingdom interactions. Nat Rev Microbiol 19, 391–404 (2021). https://doi.org/10.1038/s41579-020-00508-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41579-020-00508-1

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology