Effect of bacterial intra-species community interactions on the production and activity of volatile organic compounds
Jianing Wang, Xinlan Mei, Zhong Wei, Waseem Raza, Qirong Shen
Effect of bacterial intra-species community interactions on the production and activity of volatile organic compounds
Microorganisms experience intra- and inter-species interactions in the soil, and how these interactions affect the production of microbial volatile organic compounds (VOCs) is still not well-known. Here we evaluated the production and activity of microbial VOCs as driven by bacterial intra-species community interactions. We set up bacterial communities of increasing biodiversity out of 1–4 strains each of the Gram-positive Bacillus and Gram-negative Pseudomonas genera. We evaluated the ability of each community to provide two VOC-mediated services, pathogen suppression and plant-growth promotion and then correlated these services to the production of VOCs by each community. The results showed that an increase in community richness from 1 to 4 strains of both genera increased VOC-mediated pathogen suppression and plant-growth promotion on agar medium and in the soil, which was positively correlated with the production of pathogen suppressing and plant growth-promoting VOCs. Pseudomonas strains maintained while Bacillus strains reduced community productivity with an increase in community richness and produced eight novel VOCs compared with the monocultures. These results revealed that intra-species interactions may vary between Gram-negative and Gram-positive species but improved VOC-mediated functioning with respect to pathogen suppression and plant-growth promotion by affecting the amount and diversity of produced VOCs potentially affecting plant disease outcomes.
Biodiversity / Community richness / Ecosystem functioning / Intra-species interactions / Plant-microbe interactions
[1] |
Becker, J., Eisenhauer, N., Scheu, S., Jousset, A., 2012. Increasing antagonistic interactions cause bacterial communities to collapse at high diversity. Ecology Letters 15, 468–474
CrossRef
Google scholar
|
[2] |
Bell, T., Lilley, A.K., Hector, A., Schmid, B., King, L., Newman, J.A., 2009. A linear model method for biodiversity-ecosystem functioning experiments. American Naturalist 174, 836–849
CrossRef
Google scholar
|
[3] |
Dubuis, C., Haas, D., 2007. Cross-species GacA-controlled induction of antibiosis in Pseudomonads. Applied and Environmental Microbiology 73, 650–654
CrossRef
Google scholar
|
[4] |
Garbeva, P., Hol, W.H.G., Termorshuizen, A.J., Kowalchuk, G.A., de Boer, W., 2011. Fungistasis and general soil biostasis-a new synthesis. Soil Biology & Biochemistry 43, 469–477
CrossRef
Google scholar
|
[5] |
Gu, Y.Q., Mo, M.H., Zhou, J.P., Zou, C.S., Zhang, K.Q., 2007. Evaluation and identification of potential organic nematicidal volatiles from soil bacteria. Soil Biology & Biochemistry 39, 2567–2575
CrossRef
Google scholar
|
[6] |
Haas, D., Keel, C., 2003. Regulation of antibiotic production in root-colonizing Peudomonas spp. and relevance for biological control of plant disease. Annual Review of Phytopathology 41, 117–153
CrossRef
Google scholar
|
[7] |
Harwood, C.R., Cutting, S.M., 1990. Chemically defined growth media and supplements. In: Harwood, C.R., Cutting, S.M., eds. Molecular Biological Methods for Bacillus. Chichester: Wiley, p. 548
|
[8] |
Hazard, C., Kruitbos, L., Davidson, H., Mbow, F.T., Taylor, A.F.S., Johnson, D., 2017. Strain identity of the ectomycorrhizal fungus Laccaria bicolor is more important than richness in regulating plant and fungal performance under nutrient rich conditions. Frontiers in Microbiology 8, 1874
CrossRef
Google scholar
|
[9] |
Hu, J., Wei, Z., Weidner, S., Friman, V.P., Xu, Y.C., Shen, Q.R., Jousset, A., 2017. Probiotic Pseudomonas communities enhance plant growth and nutrient assimilation via diversity-mediated ecosystem functioning. Soil Biology & Biochemistry 1113, 122–129
CrossRef
Google scholar
|
[10] |
Jousset, A., Becker, J., Chatterjee, S., Karlovsky, P., Scheu, S., Eisenhauer, N., 2014. Biodiversity and species identity shape the antifungal activity of bacterial communities. Ecology 95, 1184–1190
CrossRef
Google scholar
|
[11] |
Jousset, A., Schmid, B., Scheu, S., Eisenhauer, N., 2011. Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecology Letters 14, 537–545
CrossRef
Google scholar
|
[12] |
Jurburg, S.D., Salles, J.F., 2015. Functional redundancy and ecosystem function — the soil microbiota as a case study. In: Lo,Y.H., Blanco, J.A., Roy, S., eds. Biodiversity Ecosystems-Linking Structure and Function. Rijeka: InTech, pp. 29–49.
|
[13] |
Kanchiswamy, C.N., Malnoy, M., Maffei, M.E., 2015. Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Frontiers of Plant Science 6, 151
CrossRef
Google scholar
|
[14] |
Lazazzara, V., Perazzolli, M., Pertot, I., Biasioli, F., Puopolo, G., Cappellin, L., 2017. Growth media affect the volatilome and antimicrobial activity against Phytophthora infestans in four Lysobacter type strains. Microbiological Research 201, 52–62
CrossRef
Google scholar
|
[15] |
Leff, J.W., Fierer, N., 2008. Volatile organic compound (VOC) emissions from soil and litter samples. Soil Biology & Biochemistry 40, 1629–1636
CrossRef
Google scholar
|
[16] |
Liu, A., Archer, A.M., Biggs, M.B., Papin, J.A., 2017. Growth-altering microbial interactions are responsive to chemical context. PLoS One 12, e0164919
CrossRef
Google scholar
|
[17] |
Loreau, M., Hector, A., 2001. Partitioning selection and complementarity in biodiversity experiments. Nature 412, 72–76
CrossRef
Google scholar
|
[18] |
Maitra, A., Dill, K.A., 2015. Bacterial growth laws reflect the evolutionary importance of energy efficiency. Proceedings of the National Academy of Sciences of the United States of America 112, 406–411
CrossRef
Google scholar
|
[19] |
Mendes, L.W., Brossi, M.J.L., Kuramae, E.E., Tsai, S.M., 2015. Land-use system shapes soil bacterial communities in Southeastern Amazon region. Applied Soil Ecology 95, 151–160
CrossRef
Google scholar
|
[20] |
Raza, W., Wang, J., Jousset, A., Friman, V.P., Mei, X., Wang, S., Wei, Z., Shen, Q., 2020. Bacterial community richness shifts the balance between volatile organic compound-mediated microbe-pathogen and microbe-plant interactions. Proceedings. Biological Sciences 287, 20200403
CrossRef
Google scholar
|
[21] |
Raza, W., Wang, J., Wu, Y., Ling, N., Wei, Z., Huang, Q., Shen, Q.R., 2016. Effects of volatile organic compounds produced by Bacillus amyloliquefaciens on the growth and virulence traits of tomato bacterial wilt pathogen Ralstonia solanacearum. Applied Microbiology and Biotechnology 100, 7639–7650
CrossRef
Google scholar
|
[22] |
Raza, W., Yuan, J., Ling, N., Huang, Q., Shen, Q., 2015. Production of volatile organic compounds by an antagonistic strain Paenibacillus polymyxa WR-2 in the presence of root exudates and organic fertilizer and their antifungal activity against Fusarium oxysporum f. sp. niveum. Biological Control 80, 89–95
CrossRef
Google scholar
|
[23] |
Rojo, F., 2010. Carbon catabolite repression in Pseudomonas: optimizing metabolic versatility and interactions with the environment. FEMS Microbiology Reviews 34, 658–684
CrossRef
Google scholar
|
[24] |
Schmidt, R., Cordovez, V., de Boer, W., Raaijmakers, J., Garbeva, P., 2015. Volatile affairs in microbial interactions. ISME Journal 9, 2329–2335
CrossRef
Google scholar
|
[25] |
Schulz, S., Dickschat, J.S., 2007. Bacterial volatiles: the smell of small organisms. Natural Product Reports 24, 814–842
CrossRef
Google scholar
|
[26] |
Schulz-Bohm, K., Zweers, H., de Boer, W., Garbeva, P., 2015. A fragrant neighborhood: volatile mediated bacterial interactions in soil. Frontiers in Microbiology 6, 1212
CrossRef
Google scholar
|
[27] |
Tahir, H.A., Gu, Q., Wu, H., Raza, W., Hanif, A., Wu, L., Colman, M.V., Gao, X., 2017. Plant growth-promotion by volatile organic compounds produced by Bacillus subtilis SYST2. Frontiers in Microbiology 8, 171
CrossRef
Google scholar
|
[28] |
Tyc, O., Zweers, H., de Boer, W., Garbeva, P., 2015. Volatiles in inter-specific bacterial interactions. Frontiers in Microbiology 6, 1412
CrossRef
Google scholar
|
[29] |
Wagg, C., Jansa, J., Schmid, B., van der Heijden, M.G.A., 2011. Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecology Letters 14, 1001–1009
CrossRef
Google scholar
|
[30] |
Wei, Z., Yang, X.M., Yin, S.X., Shen, Q., Ran, W., Xu, Y., 2011. Efficacy of Bacillus-fortified organic fertiliser in controlling bacterial wilt of tomato in the field. Applied Soil Ecology 48, 152–159
CrossRef
Google scholar
|
[31] |
Westhoff, S., van Wezel, G.P., Rozen, D.E., 2017. Distance-dependent danger responses in bacteria. Current Opinion in Microbiology 36, 95–101
CrossRef
Google scholar
|
/
〈 | 〉 |