1932

Abstract

Bacteria produce a multitude of volatile compounds. While the biological functions of these deceptively simple molecules are unknown in many cases, for compounds that have been characterized, it is clear that they serve impressively diverse purposes. Here, we highlight recent studies that are uncovering the volatile repertoire of bacteria, and the functional relevance and impact of these molecules. We present work showing the ability of volatile compounds to modulate nutrient availability in the environment; alter the growth, development, and motility of bacteria and fungi; influence protist and arthropod behavior; and impact plant and animal health. We further discuss the benefits associated with using volatile compounds for communication and competition, alongside the challenges of studying these molecules and their functional roles. Finally, we address the opportunities these compounds present from commercial, clinical, and agricultural perspectives.

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2020-09-08
2024-10-06
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Literature Cited

  1. 1. 
    Audrain B, Farag MA, Ryu C-M, Ghigo J-M 2015. Role of bacterial volatile compounds in bacterial biology. FEMS Microbiol. Rev. 39:222–33
    [Google Scholar]
  2. 2. 
    Avalos M, Garbeva P, Raaijmakers JM, van Wezel GP 2020. Production of ammonia as a low-cost and long-distance antibiotic strategy by Streptomyces species. ISME J 14:2569–83
    [Google Scholar]
  3. 3. 
    Avalos M, van Wezel GP, Raaijmakers JM, Garbeva P 2018. Healthy scents: Microbial volatiles as new frontier in antibiotic research. Curr. Opin. Microbiol. 45:84–91
    [Google Scholar]
  4. 4. 
    Becher PG, Verschut V, Bibb MJ, Bush MJ, Molnar BP et al. 2020. Developmentally regulated volatiles geosmin and 2-methylisoborneol attract a soil arthropod to Streptomyces bacteria promoting spore dispersal. Nat. Microbiol. 5:821–29
    [Google Scholar]
  5. 5. 
    Bentley SD, Chater KF, Cerdeño-Tárraga AM, Challis GL, Thomson NR et al. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–47
    [Google Scholar]
  6. 6. 
    Bernier SP, Létoffé S, Delepierre M, Ghigo J-M 2011. Biogenic ammonia modifies antibiotic resistance at a distance in physically separated bacteria. Mol. Microbiol. 81:705–16
    [Google Scholar]
  7. 7. 
    Bitas V, Kim H-S, Bennett JW, Kang S 2013. Sniffing on microbes: diverse roles of microbial volatile organic compounds in plant health. Mol. Plant Microbe Interact. 26:835–43
    [Google Scholar]
  8. 8. 
    Brakhage AA. 2013. Regulation of fungal secondary metabolism. Nat. Rev. Microbiol. 11:21–32
    [Google Scholar]
  9. 9. 
    Briard B, Heddergott C, Latgé J-P 2016. Volatile compounds emitted by Pseudomonas aeruginosa stimulate growth of the fungal pathogen Aspergillus fumigatus. mBio 7:e00219–16
    [Google Scholar]
  10. 10. 
    Busula AO, Takken W, De Boer JG, Mukubana WR, Verhulst NO 2017. Variation in host preferences of malaria mosquitoes is mediated by skin bacterial volatiles. Med. Vet. Entomol. 31:320–26
    [Google Scholar]
  11. 11. 
    Camarena-Pozos DA, Flores-Núñez VM, López MG, López-Bucio J, Partida-Martínez LP 2019. Smells from the desert: microbial volatiles that affect plant growth and development of native and non-native plant species. Plant Cell Environ 42:1368–80
    [Google Scholar]
  12. 12. 
    Čepl J, Blahůšková A, Cvrčková F, Markoš A 2014. Ammonia produced by bacterial colonies promotes growth of ampicillin-sensitive Serratia sp. by means of antibiotic inactivation. FEMS Microbiol. Lett. 354:126–32
    [Google Scholar]
  13. 13. 
    Cheffi M, Chenari Bouket A, Alenezi FN, Luptakova L, Belka M et al. 2019. Olea europaea L. root endophyte Bacillus velezensis OEE1 counteracts oomycete and fungal harmful pathogens and harbours a large repertoire of secreted and volatile metabolites and beneficial functional genes. Microorganisms 7:314
    [Google Scholar]
  14. 14. 
    Chen Y, Gozzi K, Yan F, Chai Y 2015. Acetic acid acts as a volatile signal to stimulate bacterial biofilm formation. mBio 6:e00392–15
    [Google Scholar]
  15. 15. 
    Cho G, Kim J, Park CG, Nislow C, Weller DM, Kwak Y-S 2017. Caryolan-1-ol, an antifungal volatile produced by Streptomyces spp., inhibits the endomembrane system of fungi. Open Biol 7:170075
    [Google Scholar]
  16. 16. 
    Cordovez V, Carrion VJ, Etalo DW, Mumm R, Zhu H et al. 2015. Diversity and functions of volatile organic compounds produced by Streptomyces from a disease-suppressive soil. Front. Microbiol. 6:1081
    [Google Scholar]
  17. 17. 
    Cordovez V, Schop S, Hordijk K, de Boulois HD, Coppens F et al. 2018. Priming of plant growth promotion by volatiles of root-associated Microbacterium spp. Appl. Environ. Microbiol. 84:22e01865–18
    [Google Scholar]
  18. 18. 
    D'Alessandro M, Erb M, Ton J, Brandenburg A, Karlen D et al. 2014. Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant Cell Environ 37:813–26
    [Google Scholar]
  19. 19. 
    Davies J. 2013. Specialized microbial metabolites: functions and origins. J. Antibiot. 66:361–64
    [Google Scholar]
  20. 20. 
    De Vrieze M, Pandey P, Bucheli TD, Varadarajan AR, Ahrens CH et al. 2015. Volatile organic compounds from native potato-associated Pseudomonas as potential anti-oomycete agents. Front. Microbiol. 6:1295
    [Google Scholar]
  21. 21. 
    Di Martino P, Fursy R, Bret L, Sundararaju B, Phillips RS 2003. Indole can act as an extracellular signal to regulate biofilm formation of Escherichia coli and other indole-producing bacteria. Can. J. Microbiol. 49:443–49
    [Google Scholar]
  22. 22. 
    Dickschat JS. 2010. Quorum sensing and bacterial biofilms. Nat. Prod. Rep. 27:343–69
    [Google Scholar]
  23. 23. 
    Donohoe Dallas R, Garge N, Zhang X, Sun W, O'Connell TM et al. 2011. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab 13:517–26
    [Google Scholar]
  24. 24. 
    Effmert U, Kalderás J, Warnke R, Piechulla B 2012. Volatile mediated interactions between bacteria and fungi in the soil. J. Chem. Ecol. 38:665–703
    [Google Scholar]
  25. 25. 
    El-Halfawy OM, Valvano MA. 2013. Chemical communication of antibiotic resistance by a highly resistant subpopulation of bacterial cells. PLOS ONE 8:e68874
    [Google Scholar]
  26. 26. 
    Farag MA, Ryu C-M, Sumner LW, Paré PW 2006. GC–MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67:2262–68
    [Google Scholar]
  27. 27. 
    Fiddaman PJ, Rossall S. 1993. The production of antifungal volatiles by Bacillus subtilis. J. Appl. Microbiol 74:119–26
    [Google Scholar]
  28. 28. 
    Fincheira P, Venthur H, Mutis A, Parada M, Quiroz A 2016. Growth promotion of Lactuca sativa in response to volatile organic compounds emitted from diverse bacterial species. Microbiol. Res. 193:39–47
    [Google Scholar]
  29. 29. 
    Gaines A, Ludovice M, Xu J, Zanghi M, Meinersmann RJ et al. 2019. The dialogue between protozoa and bacteria in a microfluidic device. PLOS ONE 14:e0222484
    [Google Scholar]
  30. 30. 
    Garbeva P, Hordijk C, Gerards S, de Boer W 2014. Volatile-mediated interactions between phylogenetically different soil bacteria. Front. Microbiol. 5:289
    [Google Scholar]
  31. 31. 
    Gong A-D, Wu N-N, Kong X-W, Zhang Y-M, Hu M-J et al. 2019. Inhibitory effect of volatiles emitted from Alcaligenes faecalis N1–4 on Aspergillus flavus and aflatoxins in storage. Front. Microbiol. 10:1419
    [Google Scholar]
  32. 32. 
    Groenhagen U, Baumgartner R, Bailly A, Gardiner A, Eberl L et al. 2013. Production of bioactive volatiles by different Burkholderia ambifaria strains. J. Chem. Ecol. 39:892–906
    [Google Scholar]
  33. 33. 
    Gusarov I, Nudler E. 2005. NO-mediated cytoprotection: Instant adaptation to oxidative stress in bacteria. PNAS 102:13855–60
    [Google Scholar]
  34. 34. 
    Gusarov I, Shatalin K, Starodubtseva M, Nudler E 2009. Endogenous nitric oxide protects bacteria against a wide spectrum of antibiotics. Science 325:1380–84
    [Google Scholar]
  35. 35. 
    Gust B, Challis GL, Fowler K, Kieser T, Chater KF 2003. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. PNAS 100:1541–46
    [Google Scholar]
  36. 36. 
    Hagai E, Dvora R, Havkin-Blank T, Zelinger E, Porat Z et al. 2014. Surface-motility induction, attraction and hitchhiking between bacterial species promote dispersal on solid surfaces. ISME J 8:1147–51
    [Google Scholar]
  37. 37. 
    Haidar R, Roudet J, Bonnard O, Dufour MC, Corio-Costet MF et al. 2016. Screening and modes of action of antagonistic bacteria to control the fungal pathogen Phaeomoniella chlamydospora involved in grapevine trunk diseases. Microbiol. Res. 192:172–84
    [Google Scholar]
  38. 38. 
    Herrington PR, Craig JT, Sheridan JE 1987. Methyl vinyl ketone: a volatile fungistatic inhibitor from Streptomyces griseoruber. Soil Biol. Biochem 19:509–12
    [Google Scholar]
  39. 39. 
    Hunziker L, Bonisch D, Groenhagen U, Bailly A, Schulz S, Weisskopf L 2015. Pseudomonas strains naturally associated with potato plants produce volatiles with high potential for inhibition of Phytophthora infestans. Appl. Environ. Microbiol 81:821–30
    [Google Scholar]
  40. 40. 
    Insam H, Seewald MSA. 2010. Volatile organic compounds (VOCs) in soils. Biol. Fertil. Soils 46:199–213
    [Google Scholar]
  41. 41. 
    Janssens TKS, Tyc O, Besselink H, de Boer W, Garbeva P 2019. Biological activities associated with the volatile compound 2,5-bis(1-methylethyl)-pyrazine. FEMS Microbiol. Lett. 366:fnz023
    [Google Scholar]
  42. 42. 
    Jones SE, Elliot MA. 2018. ‘Exploring’ the regulation of Streptomyces growth and development. Curr. Opin. Microbiol. 42:25–30
    [Google Scholar]
  43. 43. 
    Jones SE, Ho L, Rees CA, Hill JE, Nodwell JR, Elliot MA 2017. Streptomyces exploration is triggered by fungal interactions and volatile signals. eLife 6:e21738
    [Google Scholar]
  44. 44. 
    Jones SE, Pham CA, Zambri MP, McKillip J, Carlson EE, Elliot MA 2019. Streptomyces volatile compounds influence exploration and microbial community dynamics by altering iron availability. mBio 10:e00171-19
    [Google Scholar]
  45. 45. 
    Kai M, Effmert U, Piechulla B 2016. Bacterial-plant-interactions: approaches to unravel the biological function of bacterial volatiles in the rhizosphere. Front. Microbiol. 7:108
    [Google Scholar]
  46. 46. 
    Kanchiswamy CN, Malnoy M, Maffei ME 2015. Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front. Plant Sci. 6:151
    [Google Scholar]
  47. 47. 
    Kim K-S, Lee S, Ryu C-M 2013. Interspecific bacterial sensing through airborne signals modulates locomotion and drug resistance. Nat. Commun. 4:1809
    [Google Scholar]
  48. 48. 
    Ledger T, Rojas S, Timmermann T, Pinedo I, Poupin MJ et al. 2016. Volatile-mediated effects predominate in Paraburkholderia phytofirmans growth promotion and salt stress tolerance of Arabidopsis thaliana. Front. Microbiol 7:1838
    [Google Scholar]
  49. 49. 
    Lee J-H, Lee J. 2010. Indole as an intercellular signal in microbial communities. FEMS Microbiol. Rev. 34:426–44
    [Google Scholar]
  50. 50. 
    Lemfack MC, Ravella SR, Lorenz N, Kai M, Jung K et al. 2016. Novel volatiles of skin-borne bacteria inhibit the growth of Gram-positive bacteria and affect quorum-sensing controlled phenotypes of Gram-negative bacteria. Syst. Appl. Microbiol. 39:503–15
    [Google Scholar]
  51. 51. 
    Létoffé S, Audrain B, Bernier SP, Delepierre M, Ghigo J-M 2014. Aerial exposure to the bacterial volatile compound trimethylamine modifies antibiotic resistance of physically separated bacteria by raising culture medium pH. mBio 5:e00944-13
    [Google Scholar]
  52. 52. 
    Lo Cantore P, Giorgio A, Iacobellis NS 2015. Bioactivity of volatile organic compounds produced by Pseudomonas tolaasii. Front. Microbiol 6:1082
    [Google Scholar]
  53. 53. 
    Lopetuso LR, Scaldaferri F, Petito V, Gasbarrini A 2013. Commensal Clostridia: leading players in the maintenance of gut homeostasis. Gut Pathog 5:23
    [Google Scholar]
  54. 54. 
    McCain AH. 1966. A volatile antibiotic produced by Streptomyces griseus. Phytopathology 56:150
    [Google Scholar]
  55. 55. 
    Meldau DG, Meldau S, Hoang LH, Underberg S, Wünsche H, Baldwin IT 2013. Dimethyl disulfide produced by the naturally associated bacterium Bacillus sp B55 promotes Nicotiana attenuata growth by enhancing sulfur nutrition. Plant Cell 25:2731–47
    [Google Scholar]
  56. 56. 
    Méndez-Bravo A, Cortazar-Murillo EM, Guevara-Avendaño E, Ceballos-Luna O, Rodríguez-Haas B et al. 2018. Plant growth-promoting rhizobacteria associated with avocado display antagonistic activity against Phytophthora cinnamomi through volatile emissions. PLOS ONE 13:e0194665
    [Google Scholar]
  57. 57. 
    Misztal PK, Lymperopoulou DS, Adams RI, Scott RA, Lindow SE et al. 2018. Emission factors of microbial volatile organic compounds from environmental bacteria and fungi. Environ. Sci. Technol. 52:8272–82
    [Google Scholar]
  58. 58. 
    Molina-Santiago C, Daddaoua A, Fillet S, Duque E, Ramos J-L 2014. Interspecies signalling: Pseudomonas putida efflux pump TtgGHI is activated by indole to increase antibiotic resistance. Environ. Microbiol. 16:1267–81
    [Google Scholar]
  59. 59. 
    Montes Vidal D, von Rymon-Lipinski A-L, Ravella S, Groenhagen U, Herrmann J et al. 2017. Long-chain alkyl cyanides: unprecedented volatile compounds released by Pseudomonas and Micromonospora bacteria. Angew. Chem. Int. Ed. Engl. 56:4342–46
    [Google Scholar]
  60. 60. 
    Morita T, Tanaka I, Ryuda N, Ikari M, Ueno D, Someya T 2019. Antifungal spectrum characterization and identification of strong volatile organic compounds produced by Bacillus pumilus TM-R. Heliyon 5:e01817
    [Google Scholar]
  61. 61. 
    Nijland R, Burgess JG. 2010. Bacterial olfaction. Biotechnol. J. 5:974–77
    [Google Scholar]
  62. 62. 
    Ossowicki A, Jafra S, Garbeva P 2017. The antimicrobial volatile power of the rhizospheric isolate Pseudomonas donghuensis P482. PLOS ONE 12:e0174362
    [Google Scholar]
  63. 63. 
    Peñuelas J, Asensio D, Tholl D, Wenke K, Rosenkranz M et al. 2014. Biogenic volatile emissions from the soil. Plant Cell Environ 37:1866–91
    [Google Scholar]
  64. 64. 
    Piechulla B, Lemfack MC, Kai M 2017. Effects of discrete bioactive microbial volatiles on plants and fungi. Plant Cell Environ 40:2042–67
    [Google Scholar]
  65. 65. 
    Ping L, Boland W. 2004. Signals from the underground: Bacterial volatiles promote growth in Arabidopsis. Trends Plant Sci 9:263–66
    [Google Scholar]
  66. 66. 
    Plyuta V, Lipasova V, Popova A, Koksharova O, Kuznetsov A et al. 2016. Influence of volatile organic compounds emitted by Pseudomonas and Serratia strains on Agrobacterium tumefaciens biofilms. APMIS 124:586–94
    [Google Scholar]
  67. 67. 
    Que Y-A, Hazan R, Strobel B, Maura D, He J et al. 2013. A quorum sensing small volatile molecule promotes antibiotic tolerance in bacteria. PLOS ONE 8:e80140
    [Google Scholar]
  68. 68. 
    Ratajczak W, Ryl A, Mizerski A, Walczakiewicz K, Sipak O, Laszczynska M 2019. Immunomodulatory potential of gut microbiome-derived short-chain fatty acids (SCFAs). Acta Biochim. Pol. 66:1–12
    [Google Scholar]
  69. 69. 
    Raza W, Ling N, Liu D, Wei Z, Huang Q, Shen Q 2016. Volatile organic compounds produced by Pseudomonas fluorescens WR-1 restrict the growth and virulence traits of Ralstonia solanacearum. Microbiol. Res 192:103–13
    [Google Scholar]
  70. 70. 
    Raza W, Wang J, Wu Y, Ling N, Wei Z et al. 2016. Effects of volatile organic compounds produced by Bacillus amyloliquefaciens on the growth and virulence traits of tomato bacterial wilt pathogen Ralstonia solanacearum. Appl. Microbiol. Biotechnol 100:7639–50
    [Google Scholar]
  71. 71. 
    Rojas-Solís D, Zetter-Salmón E, Contreras-Pérez M, Rocha-Granados MDC, Macías-Rodríguez L, Santoyo G 2018. Pseudomonas stutzeri E25 and Stenotrophomonas maltophilia CR71 endophytes produce antifungal volatile organic compounds and exhibit additive plant growth-promoting effects. Biocatal. Agric. Biotechnol. 13:46–52
    [Google Scholar]
  72. 72. 
    Rudrappa T, Biedrzycki ML, Kunjeti SG, Donofrio NM, Czymmek KJ et al. 2010. The rhizobacterial elicitor acetoin induces systemic resistance in Arabidopsis thaliana. Commun. Integr. Biol 3:130–38
    [Google Scholar]
  73. 73. 
    Rybakova D, Rack-Wetzlinger U, Cernava T, Schaefer A, Schmuck M, Berg G 2017. Aerial warfare: a volatile dialogue between the plant pathogen Verticillium longisporum and its antagonist Paenibacillus polymyxa. Front. Plant Sci 8:1294
    [Google Scholar]
  74. 74. 
    Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Paré PW 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–26
    [Google Scholar]
  75. 75. 
    Sagar NM, Cree IA, Covington JA, Arasaradnam RP 2015. The interplay of the gut microbiome, bile acids, and volatile organic compounds. Gastroenterol. Res. Pract. 2015:398585
    [Google Scholar]
  76. 76. 
    Schenkel D, Lemfack M, Piechulla B, Splivallo R 2015. A meta-analysis approach for assessing the diversity and specificity of belowground root and microbial volatiles. Front. Plant Sci. 6:707
    [Google Scholar]
  77. 77. 
    Schmidt R, Cordovez V, de Boer W, Raaijmakers J, Garbeva P 2015. Volatile affairs in microbial interactions. ISME J 9:2329–35
    [Google Scholar]
  78. 78. 
    Schmidt R, Etalo DW, de Jager V, Gerards S, Zweers H et al. 2016. Microbial small talk: volatiles in fungal–bacterial interactions. Front. Microbiol. 6:1495
    [Google Scholar]
  79. 79. 
    Schmidtberg H, Shukla SP, Halitschke R, Vogel H, Vilcinskas A 2019. Symbiont-mediated chemical defense in the invasive ladybird Harmonia axyridis. Ecol. Evol 9:1715–29
    [Google Scholar]
  80. 80. 
    Schulz S, Dickschat JS. 2007. Bacterial volatiles: the smell of small organisms. Nat. Prod. Rep. 24:814–42
    [Google Scholar]
  81. 81. 
    Schulz-Bohm K, Geisen S, Wubs ERJ, Song C, de Boer W, Garbeva P 2017. The prey's scent—volatile organic compound mediated interactions between soil bacteria and their protist predators. ISME J 11:817–20
    [Google Scholar]
  82. 82. 
    Schulz-Bohm K, Martín-Sánchez L, Garbeva P 2017. Microbial volatiles: small molecules with an important role in intra- and inter-kingdom interactions. Front. Microbiol. 8:2484
    [Google Scholar]
  83. 83. 
    Schulz-Bohm K, Zweers H, de Boer W, Garbeva P 2015. A fragrant neighborhood: volatile mediated bacterial interactions in soil. Front. Microbiol. 6:1212
    [Google Scholar]
  84. 84. 
    Scott J, Sueiro-Olivares M, Ahmed W, Heddergott C, Zhao C et al. 2019. Pseudomonas aeruginosa-derived volatile sulfur compounds promote distal Aspergillus fumigatus growth and a synergistic pathogen-pathogen interaction that increases pathogenicity in co-infection. Front. Microbiol. 10:2311
    [Google Scholar]
  85. 85. 
    Shatalin K, Shatalina E, Mironov A, Nudler E 2011. H2S: a universal defense against antibiotics in bacteria. Science 334:986–90
    [Google Scholar]
  86. 86. 
    Shirata A. 1996. Production of volatile components by Pseudomonas tolaasii and their toxic activity. Jpn. J. Phytopathol. 62:185–93
    [Google Scholar]
  87. 87. 
    Smith DJ, Burnham MK, Bull JH, Hodgson JE, Ward JM et al. 1990. Beta-lactam antibiotic biosynthetic genes have been conserved in clusters in prokaryotes and eukaryotes. EMBO J 9:741–47
    [Google Scholar]
  88. 88. 
    Spraker JE, Jewell K, Roze LV, Scherf J, Ndagano D et al. 2014. A volatile relationship: profiling an inter-kingdom dialogue between two plant pathogens, Ralstonia solanacearum and Aspergillus flavus. J. Chem. Ecol 40:502–13
    [Google Scholar]
  89. 89. 
    Stensmyr MC, Dweck Hany KM, Farhan A, Ibba I, Strutz A et al. 2012. A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151:1345–57
    [Google Scholar]
  90. 90. 
    Tahir HAS, Gu Q, Wu H, Raza W, Safdar A et al. 2017. Effect of volatile compounds produced by Ralstonia solanacearum on plant growth promoting and systemic resistance inducing potential of Bacillus volatiles. BMC Plant Biol 17:133
    [Google Scholar]
  91. 91. 
    Theis KR, Schmidt TM, Holekamp KE 2012. Evidence for a bacterial mechanism for group-specific social odors among hyenas. Sci. Rep. 2:615
    [Google Scholar]
  92. 92. 
    Theis KR, Venkataraman A, Dycus JA, Koonter KD, Schmitt-Matzen EN et al. 2013. Symbiotic bacteria appear to mediate hyena social odors. PNAS 110:19832–37
    [Google Scholar]
  93. 93. 
    Tyagi S, Kim K, Cho M, Lee KJ 2019. Volatile dimethyl disulfide affects root system architecture of Arabidopsis via modulation of canonical auxin signaling pathways. Environ. Sustainability 2:211–16
    [Google Scholar]
  94. 94. 
    Tyc O, de Jager VCL, van den Berg M, Gerards S, Janssens TKS et al. 2017. Exploring bacterial interspecific interactions for discovery of novel antimicrobial compounds. Microb. Biotechnol. 10:910–25
    [Google Scholar]
  95. 95. 
    Tyc O, Zweers H, de Boer W, Garbeva P 2015. Volatiles in inter-specific bacterial interactions. Front. Microbiol. 6:1412
    [Google Scholar]
  96. 96. 
    Venkataraman A, Rosenbaum MA, Werner JJ, Winans SC, Angenent LT 2014. Metabolite transfer with the fermentation product 2,3-butanediol enhances virulence by Pseudomonas aeruginosa. ISME J 8:1210–20
    [Google Scholar]
  97. 97. 
    Veraart AJ, Garbeva P, van Beersum F, Ho A, Hordijk CA et al. 2018. Living apart together—bacterial volatiles influence methanotrophic growth and activity. ISME J 12:1163–66
    [Google Scholar]
  98. 98. 
    Verhulst NO, Andriessen R, Groenhagen U, Bukovinszkiné Kiss G, Schulz S et al. 2011. Differential attraction of malaria mosquitoes to volatile blends produced by human skin bacteria. PLOS ONE 5:e15829
    [Google Scholar]
  99. 99. 
    Verhulst NO, Qiu YT, Beijleveld H, Maliepaard C, Knights D et al. 2011. Composition of human skin microbiota affects attractiveness to malaria mosquitoes. PLOS ONE 6:e28991
    [Google Scholar]
  100. 100. 
    Werner S, Polle A, Brinkmann N 2016. Belowground communication: impacts of volatile organic compounds (VOCs) from soil fungi on other soil-inhabiting organisms. Appl. Microbiol. Biotechnol. 100:8651–65
    [Google Scholar]
  101. 101. 
    Whittaker DJ, Gerlach NM, Soini HA, Novotny MV, Ketterson ED 2013. Bird odour predicts reproductive success. Anim. Behav. 86:697–703
    [Google Scholar]
  102. 102. 
    Whittaker DJ, Slowinski SP, Greenberg JM, Alian O, Winters AD et al. 2019. Experimental evidence that symbiotic bacteria produce chemical cues in a songbird. J. Exp. Biol. 222:jeb202978
    [Google Scholar]
  103. 103. 
    Xing M, Zheng L, Deng Y, Xu D, Xi P et al. 2018. Antifungal activity of natural volatile organic compounds against litchi downy blight pathogen Peronophythora litchii. Molecules 23:358
    [Google Scholar]
  104. 104. 
    Zetola NM, Modongo C, Matsiri O, Tamuhla T, Mbongwe B et al. 2017. Diagnosis of pulmonary tuberculosis and assessment of treatment response through analyses of volatile compound patterns in exhaled breath samples. J. Infect. 74:367–76
    [Google Scholar]
  105. 105. 
    Zhou F, Xu L, Wang S, Wang B, Lou Q et al. 2017. Bacterial volatile ammonia regulates the consumption sequence of d-pinitol and d-glucose in a fungus associated with an invasive bark beetle. ISME J 11:2809–20
    [Google Scholar]
  106. 106. 
    Zhou J-Y, Li X, Zheng J-Y, Dai C-C 2016. Volatiles released by endophytic Pseudomonas fluorescens promoting the growth and volatile oil accumulation in Atractylodes lancea. Plant Physiol. Biochem 101:132–40
    [Google Scholar]
  107. 107. 
    Zou C-S, Mo M-H, Gu Y-Q, Zhou J-P, Zhang K-Q 2007. Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol. Biochem. 39:2371–79
    [Google Scholar]
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