Global-scale analysis reveals distinct patterns of non-ribosomal peptide and polyketide synthase encoding genes in root and soil bacterial communities

Barak Dror, Edouard Jurkevitch, Eddie Cytryn

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Soil Ecology Letters ›› 2023, Vol. 5 ›› Issue (1) : 38-45. DOI: 10.1007/s42832-022-0146-2
RESEARCH ARTICLE
RESEARCH ARTICLE

Global-scale analysis reveals distinct patterns of non-ribosomal peptide and polyketide synthase encoding genes in root and soil bacterial communities

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Highlights

● The overall abundance of secondary metabolites-encoding genes in soil and root microbiomes is similar.

● Certain biosynthetic gene clusters (BGCs) are ubiquitous and more abundant in roots compared with soil.

● The majority of identified BGCs are potentially novel.

Abstract

Secondary metabolites (SMs) produced by soil bacteria, for instance antimicrobials and siderophores, play a vital role in bacterial adaptation to soil and root ecosystems and can contribute to plant health. Many SMs are non-ribosomal peptides and polyketides, assembled by non-ribosomal peptides synthetase (NRPS) and polyketide synthase (PKS) and encoded by biosynthetic gene clusters (BGCs). Despite their ecological importance, little is known about the occurrence and diversity of NRPs and PKs in soil. We extracted NRPS- and PKS-encoding BGCs from 20 publicly available soil and root-associated metagenomes and annotated them using antiSMASH-DB. We found that the overall abundance of NRPSs and PKSs is similar in both environments, however NRPSs and PKSs were significantly clustered between soil and root samples. Moreover, the majority of identified sequences were unique to either soil- or root-associated datasets and had low identity to known BGCs, suggesting their novelty. Overall, this study illuminates the huge untapped diversity of predicted SMs in soil and root microbiomes, and indicates presence of specific SMs, which may play a role in inter- and intra-bacterial interactions in root ecosystems.

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Keywords

Secondary metabolites / Plant-microbe interactions / Non-ribosomal peptides / Polyketides / Rhizosphere microbiome / Soil microbiome

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Barak Dror, Edouard Jurkevitch, Eddie Cytryn. Global-scale analysis reveals distinct patterns of non-ribosomal peptide and polyketide synthase encoding genes in root and soil bacterial communities. Soil Ecology Letters, 2023, 5(1): 38‒45 https://doi.org/10.1007/s42832-022-0146-2

References

[1]
Amos, G.C.A., Borsetto, C., Laskaris, P., Krsek, M., Berry, A.E., Newsham, K.K., Calvo-Bado, L., Pearce, D.A., Vallin, C., Wellington, E.M.H., 2015. Designing and implementing an assay for the detection of rare and divergent NRPS and PKS clones in European, Antarctic and Cuban soils. PLoS ONE 10, 1– 15.
[2]
Blin, K., Shaw, S., Steinke, K., Villebro, R., Ziemert, N., Lee, S.Y., Medema, M.H., Weber, T., 2019. AntiSMASH 5.0: Updates to the secondary metabolite genome mining pipeline. Nucleic Acids Research 47, W81– W87.
[3]
Bodor, A., Bounedjoum, N., Vincze, G.E., Kis, Á.E., Laczi, K., Bende, G., Szilágyi, Á., Kovács, T., Perei, K., Rákhely, G., 2020. Challenges of unculturable bacteria: environmental perspectives. Reviews in Environmental Science and Bio/Technology 19, 1– 22.
[4]
de Bruijn, I., Cheng, X., de Jager, V., Expósito, R.G., Watrous, J., Patel, N., Postma, J., Dorrestein, P.C., Kobayashi, D., Raaijmakers, J.M., 2015. Comparative genomics and metabolic profiling of the genus Lysobacter. BMC Genomics 16, 1– 16.
[5]
Charlop-Powers, Z., Pregitzer, C.C., Lemetre, C., Ternei, M.A., Maniko, J., Hover, B.M., Calle, P.Y., McGuire, K.L., Garbarino, J., Forgione, H.M., Charlop-Powers, S., Brady, S.F., 2016. Urban park soil microbiomes are a rich reservoir of natural product biosynthetic diversity. Proceedings of the National Academy of Sciences of the United States of America 113, 14811– 14816.
[6]
Cordovez, V., Dini-Andreote, F., Carrión, V.J., Raaijmakers, J.M. 2019. Ecology and evolution of plant microbiomes. Annual review of Microbiology 73, 69– 88.
[7]
Dror, B., Jurkevitch, E., Cytryn, E. 2020a. State-of-the-art methodologies to identify antimicrobial secondary metabolites in soil bacterial communities−A review. Soil Biology and Biochemistry 147, 107838.
[8]
Dror, B, Wang, Z., Brady, S.F., Jurkevitch, E., Cytryn, E., 2020b. Elucidating the diversity and potential function of nonribosomal peptide and polyketide biosynthetic gene clusters in the root microbiome. mSystems 5, e00866– 20.
[9]
Eastman, A.W., Heinrichs, D.E., Yuan, Z.C., 2014. Comparative and genetic analysis of the four sequenced Paenibacillus polymyxa genomes reveals a diverse metabolism and conservation of genes relevant to plant-growth promotion and competitiveness. BMC Genomics 15, 851.
[10]
Eckert, E.M., Di Cesare, A., Fontaneto, D., Berendonk, T.U., Bürgmann, H., Cytryn, E., Fatta-Kassinos, D., Franzetti, A., Larsson, D.G.J., Manaia, C.M., 2020. Every fifth published metagenome is not available to science. PLoS Biology 18, e3000698.
[11]
Fierer, N., Stricklandd, S., Liptzind, D., Bradford, A., Cleveland, C., 2009. Global patterns in belowground communities. Ecology Letters 12, 1– 12.
[12]
Huson, D.H., Beier, S., Flade, I., Górska, A., El-Hadidi, M., Mitra, S., Ruscheweyh, H.J., Tappu, R., 2016. MEGAN community edition-interactive exploration and analysis of large-scale microbiome sequencing data. PLoS Computational Biology 12, e1004957.
[13]
Jenke-Kodama, H., Sandmann, A., Müller, R., Dittmann, E., 2005. Evolutionary implications of bacterial polyketide synthases. Molecular Biology and Evolution 22, 2027– 2039.
[14]
Kawasaki, A., Donn, S., Ryan, P.R., Mathesius, U., Devilla, R., Jones, A., Watt, M., 2016. Microbiome and exudates of the root and rhizosphere of Brachypodium distachyon, a model for wheat. PloS One 11, e0164533.
[15]
Lee, S.A., Kim, Y., Kim, J.M., Chu, B., Joa, J.H., Sang, M.K., Song, J., Weon, H.Y., 2019. A preliminary examination of bacterial, archaeal, and fungal communities inhabiting different rhizocompartments of tomato plants under real-world environments. Scientific Reports 9, 1– 15.
[16]
Levy, A., Conway, J.M., Dangl, J.L., Woyke, T., 2018. Elucidating bacterial gene functions in the plant microbiome. Cell Host & Microbe 24, 475– 485.
[17]
McErlean, M., Overbay, J., Van Lanen, S., 2019. Refining and expanding nonribosomal peptide synthetase function and mechanism. Journal of Industrial Microbiology and Biotechnology 46, 493– 513.
[18]
Nguyen, T.M., Seo, C., Ji, M., Paik, M.J., Myung, S.W., Kim, J., 2018. Effective soil extraction method for cultivating previously uncultured soil bacteria. Applied and Environmental Microbiology 84, e01145– 18.
[19]
Noronha, M.F., Lacerda Júnior, G.V., Gilbert, J.A., de Oliveira, V.M., 2017. Taxonomic and functional patterns across soil microbial communities of global biomes. Science of The Total Environment 609, 1064– 1074.
[20]
Ofek-Lalzar, M., Sela, N., Goldman-Voronov, M., Green, S.J., Hadar, Y., Minz, D., 2014. Niche and host-associated functional signatures of the root surface microbiome. Nature Communications 5, 1– 9.
[21]
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Wagner, H., 2013. Package ‘vegan’. Community ecology package, version 2, 1– 295
[22]
Peiffer, J.A., Spor, A., Koren, O., Jin, Z., Tringe, S.G., Dangl, J.L., Buckler, E.S., Ley, R.E., 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proceedings of the National Academy of Sciences 110, 6548– 6553.
[23]
Qiao, Q., Wang, F., Zhang, J., Chen, Y., Zhang, C., Liu, G., Zhang, H., Ma, C., Zhang, J., 2017. The variation in the rhizosphere microbiome of cotton with soil type, genotype and developmental stage. Scientific Reports 7, 1– 10.
[24]
Sasse, J., Martinoia, E., Northen, T., 2018. Feed your friends: do plant exudates shape the root microbiome? Trends in Plant Science 23, 25– 41
[25]
Schlaeppi, K., Bulgarelli, D., 2015. The plant microbiome at work. Molecular Plant-microbe Interactions 28, 212– 217.
[26]
Schmidt, J.E., Kent, A.D., Brisson, V.L., Gaudin, A.C.M., 2019. Agricultural management and plant selection interactively affect rhizosphere microbial community structure and nitrogen cycling. Microbiome 7: 1– 18
[27]
Sharrar, A.M., Crits-Christoph, A., Méheust, R., Diamond, S., Starr, E.P., Banfield, J.F., 2020. Bacterial secondary metabolite biosynthetic potential in soil varies with phylum, depth, and vegetation type. Mbio 11, e00416– 20.
[28]
Tyc, O., Song, C., Dickschat, J.S., Vos, M., Garbeva, P., 2017. The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends in Microbiology 25, 280– 292.
[29]
Vangay, P., Burgin, J., Johnston, A., Beck, K.L., Berrios, D.C., Blumberg, K., Canon, S., Chain, P., Chandonia, J.M., Christianson, D., 2021. Microbiome metadata standards: report of the National Microbiome Data Collaborative’s Workshop and follow-on activities. mSystems 6, e01194– 20.
[30]
Wang, H., Fewer, D.P., Holm, L., Rouhiainen, L., Sivonen, K., 2014. Atlas of nonribosomal peptide and polyketide biosynthetic pathways reveals common occurrence of nonmodular enzymes. Proceedings of the National Academy of Sciences 111, 9259– 9264.
[31]
Waschulin, V., Borsetto, C., James, R., Newsham, K.K., Donadio, S., Corre, C., Wellington, E., 2021. Biosynthetic potential of uncultured Antarctic soil bacteria revealed through long-read metagenomic sequencing. The ISME Journal 16, 1– 11.
[32]
Yan, Y., Kuramae, E.E., De Hollander, M., Klinkhamer, P.G., Van Veen, J.A., 2017. Functional traits dominate the diversity-related selection of bacterial communities in the rhizosphere. The ISME Journal 11, 56– 66.

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Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-022-0146-2 and is accessible for authorized users.

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