Abstract
Secondary metabolites produced by microorganisms are the main source of antimicrobials and other pharmaceutical drugs. Soil microbes have been the primary discovery source for these secondary metabolites, often producing complex organic compounds with specific biological activities. Research suggests that secondary metabolism broadly shapes microbial ecological interactions, but little is known about the factors that shape the abundance, distribution, and diversity of biosynthetic gene clusters in the context of microbial communities. In this study, we investigate the role of nutrient availability on the abundance of biosynthetic gene clusters in soil-derived microbial consortia. Soil microbial consortia enriched in high sugar medium (150 mg/L of glucose and 200 mg/L of trehalose) had more biosynthetic gene clusters and higher inhibitory activity than those enriched in low sugar medium (15 mg/L of glucose + 20 mg/L of trehalose). Our results demonstrate that experimental microbial communities are a promising tool to study the ecology of specialized metabolites.
References
Netzker T, Fischer J, Weber J, Mattern DJ, König CC, Valiante V et al (2015) Microbial communication leading to the activation of silent fungal secondary metabolite gene clusters. Front Microbiol. https://doi.org/10.3389/fmicb.2015.00299
Demain AL (2014) Importance of microbial natural products and the need to revitalize their discovery. J Ind Microbiol Biotechnol 41:185–201. https://doi.org/10.1007/s10295-013-1325-z
Sharrar AM, Crits-Christoph A, Méheust R, Diamond S, Starr EP, Banfield JF et al (2020) Bacterial secondary metabolite biosynthetic potential in soil varies with phylum, depth, and vegetation type. MBio 11:e00416-00420. https://doi.org/10.1128/mBio.00416-20
Chevrette MG, Handelsman J (2021) Needles in haystacks: reevaluating old paradigms for the discovery of bacterial secondary metabolites. Nat Prod Rep. https://doi.org/10.1039/D1NP00044F
Borsetto C, Amos GCA, da Rocha UN, Mitchell AL, Finn RD, Laidi RF et al (2019) Microbial community drivers of PK/NRP gene diversity in selected global soils. Microbiome 7:78. https://doi.org/10.1186/s40168-019-0692-8
Charlop-Powers Z, Owen JG, Reddy BV, Ternei MA, Brady SF (2014) Chemical-biogeographic survey of secondary metabolism in soil. Proc Natl Acad Sci USA 111:3757–3762. https://doi.org/10.1073/pnas.1318021111
Nayfach S, Roux S, Seshadri R, Udwary D, Varghese N, Schulz F et al (2021) A genomic catalog of Earth’s microbiomes. Nat Biotechnol 39:499–509. https://doi.org/10.1038/s41587-020-0718-6
Chevrette MG, Currie CR (2019) Emerging evolutionary paradigms in antibiotic discovery. J Ind Microbiol Biotechnol 46:257–271. https://doi.org/10.1007/s10295-018-2085-6
Chevrette MG, Gutiérrez-García K, Selem-Mojica N, Aguilar-Martínez C, Yañez-Olvera A, Ramos-Aboites HE et al (2020) Evolutionary dynamics of natural product biosynthesis in bacteria. Nat Prod Rep 37:566–599. https://doi.org/10.1039/c9np00048h
Chase AB, Sweeney D, Muskat MN, Guillén-Matus D, Jensen PR (2021) Vertical inheritance governs biosynthetic gene cluster evolution and chemical diversification. bioRxiv. https://doi.org/10.1101/2020.12.19.423547
Chevrette MG, Gavrilidou A, Mantri S, Selem-Mojica N, Ziemert N, Barona-Gómez F (2021) The confluence of big data and evolutionary genome mining for the discovery of natural products. Nat Prod Rep. https://doi.org/10.1039/D1NP00013F
Okada BK, Seyedsayamdost MR (2017) Antibiotic dialogues: induction of silent biosynthetic gene clusters by exogenous small molecules. FEMS Microbiol Rev 41:19–33. https://doi.org/10.1093/femsre/fuw035
Hurley A, Chevrette MG, Acharya DD, Lozano GL, Garavito M, Heinritz J et al (2021) Tiny earth: a big idea for STEM education and antibiotic discovery. MBio. https://doi.org/10.1128/mBio.03432-20
Jenkins S, Swenson TL, Lau R, Rocha AM, Aaring A, Hazen TC et al (2017) Construction of viable soil defined media using quantitative metabolomics analysis of soil metabolites. Front Microbiol. https://doi.org/10.3389/fmicb.2017.02618
Menzel P, Ng KL, Krogh A (2016) Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun 7:11257. https://doi.org/10.1038/ncomms11257
Friedman J, Alm EJ (2012) Inferring correlation networks from genomic survey data. PLoS Comput Biol 8:e1002687. https://doi.org/10.1371/journal.pcbi.1002687
Chong J, Liu P, Zhou G, Xia J (2020) Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nat Protoc 15:799–821. https://doi.org/10.1038/s41596-019-0264-1
Nurk S, Bankevich A, Antipov D, Gurevich A, Korobeynikov A, Lapidus A et al (2013) Assembling genomes and mini-metagenomes from highly chimeric reads. Springer, Berlin, pp 158–170
Blin K, Shaw S, Steinke K, Villebro R, Ziemert N, Lee SY et al (2019) antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 47:W81–W87. https://doi.org/10.1093/nar/gkz310
von Meijenfeldt FAB, Arkhipova K, Cambuy DD, Coutinho FH, Dutilh BE (2019) Robust taxonomic classification of uncharted microbial sequences and bins with CAT and BAT. Genome Biol 20:217. https://doi.org/10.1186/s13059-019-1817-x
Fender JE, Bender CM, Stella NA, Lahr RM, Kalivoda EJ, Shanks RM (2012) Serratia marcescens quinoprotein glucose dehydrogenase activity mediates medium acidification and inhibition of prodigiosin production by glucose. Appl Environ Microbiol 78:6225–6235. https://doi.org/10.1128/aem.01778-12
Sánchez S, Chávez A, Forero A, García-Huante Y, Romero A, Sánchez M et al (2010) Carbon source regulation of antibiotic production. J Antibiot (Tokyo) 63:442–459. https://doi.org/10.1038/ja.2010.78
Cui J, Yuan X, Zhang Q, Zhou J, Lin K, Xu J et al (2021) Nutrient availability is a dominant predictor of soil bacterial and fungal community composition after nitrogen addition in subtropical acidic forests. PLoS ONE 16:e0246263. https://doi.org/10.1371/journal.pone.0246263
Reischke S, Rousk J, Bååth E (2014) The effects of glucose loading rates on bacterial and fungal growth in soil. Biol Biochem 70:88–95. https://doi.org/10.1016/j.soilbio.2013.12.011
Robey MT, Caesar LK, Drott MT, Keller NP, Kelleher NL (2021) An interpreted atlas of biosynthetic gene clusters from 1,000 fungal genomes. Proc Natl Acad Sci 118:e2020230118. https://doi.org/10.1073/pnas.2020230118
van Bergeijk DA, Terlouw BR, Medema MH, van Wezel GP (2020) Ecology and genomics of Actinobacteria: new concepts for natural product discovery. Nat Rev Microbiol 18:546–558. https://doi.org/10.1038/s41579-020-0379-y
Westhoff S, Kloosterman AM, van Hoesel SFA, van Wezel GP, Rozen DE (2021) Competition sensing changes antibiotic production in streptomyces. MBio. https://doi.org/10.1128/mBio.02729-20
Abrudan MI, Smakman F, Grimbergen AJ, Westhoff S, Miller EL, van Wezel GP et al (2015) Socially mediated induction and suppression of antibiosis during bacterial coexistence. Proc Natl Acad Sci 112:11054–11059. https://doi.org/10.1073/pnas.1504076112
Zhang C, Straight PD (2019) Antibiotic discovery through microbial interactions. Curr Opin Microbiol 51:64–71. https://doi.org/10.1016/j.mib.2019.06.006
Ueda K, Beppu T (2017) Antibiotics in microbial coculture. J Antibiot 70:361–365. https://doi.org/10.1038/ja.2016.127
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or nonprofit sectors. Support for M.G.C. was provided by grant 2020-67012-31772 (Accession 1022881) from the U.S. Department of Agriculture, National Institute of Food and Agriculture.
Author information
Authors and Affiliations
Contributions
CC-S and BH designed the experiments. BH performed the experiments. MGC and CC-S performed bioinformatic and statistical analyses. MGC, BH, and CC-S wrote and reviewed the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethical Approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chevrette, M.G., Himes, B.W. & Carlos-Shanley, C. Nutrient Availability Shifts the Biosynthetic Potential of Soil-Derived Microbial Communities. Curr Microbiol 79, 64 (2022). https://doi.org/10.1007/s00284-021-02746-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00284-021-02746-9