Bacterial Secondary Metabolite Biosynthetic Potential in Soil Varies with Phylum, Depth, and Vegetation Type

Sharrar, Allison M.; Crits-Christoph, Alexander; Méheust, Raphaël; Diamond, Spencer; Starr, Evan P.; Banfield, Jillian F.; Davies, ed., Julian E.

doi:10.1128/mBio.00416-20

Title: Bacterial Secondary Metabolite Biosynthetic Potential in Soil Varies with Phylum, Depth, and Vegetation Type

Journal Article · Tue Jun 30 00:00:00 EDT 2020 · mBio

DOI:https://doi.org/10.1128/mBio.00416-20· OSTI ID:1633383

Sharrar, Allison M. ^[1]; Crits-Christoph, Alexander ^[2]; Méheust, Raphaël ^[3]; Diamond, Spencer ^[1]; Starr, Evan P. ^[2]; Banfield, Jillian F. ^[3]; Davies, ed., Julian E.

Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, California, USA
Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, California, USA
Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, California, USA, Innovative Genomics Institute, Berkeley, California, USA

Bacteria isolated from soils are major sources of specialized metabolites, including antibiotics and other compounds with clinical value that likely shape interactions among microbial community members and impact biogeochemical cycles. Yet, isolated lineages represent a small fraction of all soil bacterial diversity. It remains unclear how the production of specialized metabolites varies across the phylogenetic diversity of bacterial species in soils and whether the genetic potential for production of these metabolites differs with soil depth and vegetation type within a geographic region. We sampled soils and saprolite from three sites in a northern California Critical Zone Observatory with various vegetation and bedrock characteristics and reconstructed 1,334 metagenome-assembled genomes containing diverse biosynthetic gene clusters (BGCs) for secondary metabolite production. We obtained genomes for prolific producers of secondary metabolites, including novel groups within the Actinobacteria, Chloroflexi, and candidate phylum “Candidatus Dormibacteraeota.” Surprisingly, one genome of a candidate phyla radiation (CPR) bacterium coded for a ribosomally synthesized linear azole/azoline-containing peptide, a capacity we found in other publicly available CPR bacterial genomes. Overall, bacteria with higher biosynthetic potential were enriched in shallow soils and grassland soils, with patterns of abundance of BGC type varying by taxonomy.

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Research Organization:: Univ. of California, Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)

Grant/Contract Number:: DOE-SC10010566; SC0010566; CZP EAR-1331940

OSTI ID:: 1633383

Alternate ID(s):: OSTI ID: 1816397

Journal Information:: mBio, Journal Name: mBio Vol. 11 Journal Issue: 3; ISSN 2161-2129

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (69)

Unexpected applications of secondary metabolites Vaishnav, Preeti; Demain, Arnold L. Biotechnology Advances, Vol. 29, Issue 2 https://doi.org/10.1016/j.biotechadv.2010.11.006	journal	March 2011
Communication in bacteria: an ecological and evolutionary perspective Keller, Laurent; Surette, Michael G. Nature Reviews Microbiology, Vol. 4, Issue 4 https://doi.org/10.1038/nrmicro1383	journal	February 2006
Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone Butterfield, Cristina N.; Li, Zhou; Andeer, Peter F. PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2687	journal	January 2016
Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas Nature Biotechnology, Vol. 35, Issue 8 https://doi.org/10.1038/nbt.3893	journal	August 2017
The distinction of CPR bacteria from other bacteria based on protein family content Méheust, Raphaël; Burstein, David; Castelle, Cindy J. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12171-z	journal	September 2019
Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes Wallenstein, Matthew D.; Weintraub, Michael N. Soil Biology and Biochemistry, Vol. 40, Issue 9 https://doi.org/10.1016/j.soilbio.2008.01.024	journal	September 2008
Natural products: A continuing source of novel drug leads Cragg, Gordon M.; Newman, David J. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1830, Issue 6 https://doi.org/10.1016/j.bbagen.2013.02.008	journal	June 2013
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
Natural Product Biosynthetic Gene Diversity in Geographically Distinct Soil Microbiomes Reddy, Boojala Vijay B.; Kallifidas, Dimitris; Kim, Jeffrey H. Applied and Environmental Microbiology, Vol. 78, Issue 10 https://doi.org/10.1128/AEM.00102-12	journal	March 2012
Urban park soil microbiomes are a rich reservoir of natural product biosynthetic diversity Charlop-Powers, Zachary; Pregitzer, Clara C.; Lemetre, Christophe Proceedings of the National Academy of Sciences, Vol. 113, Issue 51 https://doi.org/10.1073/pnas.1615581113	journal	November 2016
Genome Features and Secondary Metabolites Biosynthetic Potential of the Class Ktedonobacteria Zheng, Yu; Saitou, Ayana; Wang, Chiung-Mei Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00893	journal	April 2019
Phylogenetic Analysis of Type I and Type II Polyketide Synthase from Tropical Forest Soil Pang, Mei-Fong; Annie Tan, Geok-Yuan; Abdullah, Noorlidah Biotechnology(Faisalabad), Vol. 7, Issue 4 https://doi.org/10.3923/biotech.2008.660.668	journal	April 2008
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph Li, Dinghua; Liu, Chi-Man; Luo, Ruibang Bioinformatics, Vol. 31, Issue 10 https://doi.org/10.1093/bioinformatics/btv033	journal	January 2015
Species Interactions Reverse Grassland Responses to Changing Climate Suttle, K. B.; Thomsen, M. A.; Power, M. E. Science, Vol. 315, Issue 5812 https://doi.org/10.1126/science.1136401	journal	February 2007
Genome Mining Reveals a Minimum Gene Set for the Biosynthesis of 32-Membered Macrocyclic Thiopeptides Lactazoles Hayashi, Shohei; Ozaki, Taro; Asamizu, Shumpei Chemistry & Biology, Vol. 21, Issue 5 https://doi.org/10.1016/j.chembiol.2014.03.008	journal	May 2014
Ecological and Genomic Attributes of Novel Bacterial Taxa That Thrive in Subsurface Soil Horizons Brewer, Tess E.; Aronson, Emma L.; Arogyaswamy, Keshav mBio, Vol. 10, Issue 5 https://doi.org/10.1128/mBio.01318-19	journal	October 2019
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities Kang, Dongwan D.; Froula, Jeff; Egan, Rob PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1165	journal	January 2015
Siderophore-Based Iron Acquisition and Pathogen Control Miethke, M.; Marahiel, M. A. Microbiology and Molecular Biology Reviews, Vol. 71, Issue 3 https://doi.org/10.1128/MMBR.00012-07	journal	September 2007
Structure of ribosome-bound azole-modified peptide phazolicin rationalizes its species-specific mode of bacterial translation inhibition Travin, Dmitrii Y.; Watson, Zoe L.; Metelev, Mikhail Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12589-5	journal	October 2019
MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets Wu, Yu-Wei; Simmons, Blake A.; Singer, Steven W. Bioinformatics, Vol. 32, Issue 4 https://doi.org/10.1093/bioinformatics/btv638	journal	October 2015
antiSMASH 4.0—improvements in chemistry prediction and gene cluster boundary identification Blin, Kai; Wolf, Thomas; Chevrette, Marc G. Nucleic Acids Research, Vol. 45, Issue W1 https://doi.org/10.1093/nar/gkx319	journal	April 2017
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
Dissection of goadsporin biosynthesis by in vitro reconstitution leading to designer analogues expressed in vivo Ozaki, Taro; Yamashita, Kona; Goto, Yuki Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14207	journal	February 2017
Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations Castelle, Cindy J.; Brown, Christopher T.; Anantharaman, Karthik Nature Reviews Microbiology, Vol. 16, Issue 10 https://doi.org/10.1038/s41579-018-0076-2	journal	September 2018
BiosyntheticSPAdes: reconstructing biosynthetic gene clusters from assembly graphs Meleshko, Dmitry; Mohimani, Hosein; Tracanna, Vittorio Genome Research, Vol. 29, Issue 8 https://doi.org/10.1101/gr.243477.118	journal	June 2019
Microbial community drivers of PK/NRP gene diversity in selected global soils Borsetto, Chiara; Amos, Gregory C. A.; da Rocha, Ulisses Nunes Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0692-8	journal	May 2019
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
Chemical-biogeographic survey of secondary metabolism in soil Charlop-Powers, Zachary; Owen, Jeremy G.; Reddy, Boojala Vijay B. Proceedings of the National Academy of Sciences, Vol. 111, Issue 10 https://doi.org/10.1073/pnas.1318021111	journal	February 2014
Drainage from the Critical Zone: Lithologic Controls on the Persistence and Spatial Extent of Wetted Channels during the Summer Dry Season Lovill, S. M.; Hahm, W. J.; Dietrich, W. E. Water Resources Research, Vol. 54, Issue 8 https://doi.org/10.1029/2017WR021903	journal	August 2018
Diversity and abundance of phosphonate biosynthetic genes in nature Yu, X.; Doroghazi, J. R.; Janga, S. C. Proceedings of the National Academy of Sciences, Vol. 110, Issue 51 https://doi.org/10.1073/pnas.1315107110	journal	December 2013
Lasso Peptides: An Intriguing Class of Bacterial Natural Products Hegemann, Julian D.; Zimmermann, Marcel; Xie, Xiulan Accounts of Chemical Research, Vol. 48, Issue 7 https://doi.org/10.1021/acs.accounts.5b00156	journal	June 2015
Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy Sieber, Christian M. K.; Probst, Alexander J.; Sharrar, Allison Nature Microbiology, Vol. 3, Issue 7 https://doi.org/10.1038/s41564-018-0171-1	journal	May 2018
Quorum Sensing Modulates the Epibiotic-Parasitic Relationship Between Actinomyces odontolyticus and Its Saccharibacteria epibiont, a Nanosynbacter lyticus Strain, TM7x Bedree, Joseph K.; Bor, Batbileg; Cen, Lujia Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02049	journal	September 2018
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts174	journal	April 2012
Bacterial competition: surviving and thriving in the microbial jungle Hibbing, Michael E.; Fuqua, Clay; Parsek, Matthew R. Nature Reviews Microbiology, Vol. 8, Issue 1 https://doi.org/10.1038/nrmicro2259	journal	November 2009
Novel soil bacteria possess diverse genes for secondary metabolite biosynthesis Crits-Christoph, Alexander; Diamond, Spencer; Butterfield, Cristina N. Nature, Vol. 558, Issue 7710 https://doi.org/10.1038/s41586-018-0207-y	journal	June 2018
Marine Sponges as Chloroflexi Hot Spots: Genomic Insights and High-Resolution Visualization of an Abundant and Diverse Symbiotic Clade Bayer, Kristina; Jahn, Martin T.; Slaby, Beate M. mSystems, Vol. 3, Issue 6 https://doi.org/10.1128/mSystems.00150-18	journal	December 2018
The Pfam protein families database in 2019 El-Gebali, Sara; Mistry, Jaina; Bateman, Alex Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky995	journal	October 2018
Mediterranean grassland soil C–N compound turnover is dependent on rainfall and depth, and is mediated by genomically divergent microorganisms Diamond, Spencer; Andeer, Peter F.; Li, Zhou Nature Microbiology, Vol. 4, Issue 8 https://doi.org/10.1038/s41564-019-0449-y	journal	May 2019
ModelFinder: fast model selection for accurate phylogenetic estimates Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F. Nature Methods, Vol. 14, Issue 6 https://doi.org/10.1038/nmeth.4285	journal	May 2017
UniProt: the Universal Protein knowledgebase Apweiler, R. Nucleic Acids Research, Vol. 32, Issue 90001 https://doi.org/10.1093/nar/gkh131	journal	January 2004
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
Binning metagenomic contigs by coverage and composition Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino Nature Methods, Vol. 11, Issue 11 https://doi.org/10.1038/nmeth.3103	journal	September 2014
Anaerobic Ammonium-Oxidizing Bacteria: Unique Microorganisms with Exceptional Properties van Niftrik, L.; Jetten, M. S. M. Microbiology and Molecular Biology Reviews, Vol. 76, Issue 3 https://doi.org/10.1128/MMBR.05025-11	journal	August 2012
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Creating the CIPRES Science Gateway for inference of large phylogenetic trees Miller, Mark A.; Pfeiffer, Wayne; Schwartz, Terri 2010 Gateway Computing Environments Workshop (GCE) https://doi.org/10.1109/GCE.2010.5676129	conference	November 2010
Discovery, Biosynthesis, and Engineering of Lantipeptides Knerr, Patrick J.; van der Donk, Wilfred A. Annual Review of Biochemistry, Vol. 81, Issue 1 https://doi.org/10.1146/annurev-biochem-060110-113521	journal	July 2012
Controls on the distribution and resilience of Quercus garryana : ecophysiological evidence of oak's water-limitation tolerance Hahm, W. Jesse; Dietrich, William E.; Dawson, Todd E. Ecosphere, Vol. 9, Issue 5 https://doi.org/10.1002/ecs2.2218	journal	May 2018
Bacterial natural product biosynthetic domain composition in soil correlates with changes in latitude on a continent-wide scale Lemetre, Christophe; Maniko, Jeffrey; Charlop-Powers, Zachary Proceedings of the National Academy of Sciences, Vol. 114, Issue 44 https://doi.org/10.1073/pnas.1710262114	journal	October 2017
A new view of the tree of life Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.48	journal	April 2016
Investigation of Proposed Ladderane Biosynthetic Genes from Anammox Bacteria by Heterologous Expression in E. coli Javidpour, Pouya; Deutsch, Samuel; Mutalik, Vivek K. PLOS ONE, Vol. 11, Issue 3 https://doi.org/10.1371/journal.pone.0151087	journal	March 2016
dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication Olm, Matthew R.; Brown, Christopher T.; Brooks, Brandon The ISME Journal, Vol. 11, Issue 12 https://doi.org/10.1038/ismej.2017.126	journal	July 2017
Quantification of the seasonal hillslope water storage that does not drive streamflow: Catchment storage that does not drive streamflow Dralle, David N.; Hahm, W. Jesse; Rempe, Daniella M. Hydrological Processes, Vol. 32, Issue 13 https://doi.org/10.1002/hyp.11627	journal	May 2018
YcaO-Dependent Posttranslational Amide Activation: Biosynthesis, Structure, and Function Burkhart, Brandon J.; Schwalen, Christopher J.; Mann, Greg Chemical Reviews, Vol. 117, Issue 8 https://doi.org/10.1021/acs.chemrev.6b00623	journal	March 2017
Lithologically Controlled Subsurface Critical Zone Thickness and Water Storage Capacity Determine Regional Plant Community Composition Hahm, W. Jesse; Rempe, Daniella M.; Dralle, David N. Water Resources Research, Vol. 55, Issue 4 https://doi.org/10.1029/2018WR023760	journal	April 2019
Direct observations of rock moisture, a hidden component of the hydrologic cycle Rempe, Daniella M.; Dietrich, William E. Proceedings of the National Academy of Sciences, Vol. 115, Issue 11 https://doi.org/10.1073/pnas.1800141115	journal	February 2018
The Ecological Role of Volatile and Soluble Secondary Metabolites Produced by Soil Bacteria Tyc,, Olaf; Song, Chunxu; Dickschat, Jeroen S. Trends in Microbiology, Vol. 25, Issue 4 https://doi.org/10.1016/j.tim.2016.12.002	journal	April 2017
A simple method to control over-alignment in the MAFFT multiple sequence alignment program Katoh, Kazutaka; Standley, Daron M. Bioinformatics, Vol. 32, Issue 13 https://doi.org/10.1093/bioinformatics/btw108	journal	February 2016
The Biogeography of Putative Microbial Antibiotic Production Morlon, Hélène; O'Connor, Timothy K.; Bryant, Jessica A. PLOS ONE, Vol. 10, Issue 6 https://doi.org/10.1371/journal.pone.0130659	journal	June 2015
Digging deeper to find unique microbial communities: The strong effect of depth on the structure of bacterial and archaeal communities in soil Eilers, Kathryn G.; Debenport, Spencer; Anderson, Suzanne Soil Biology and Biochemistry, Vol. 50 https://doi.org/10.1016/j.soilbio.2012.03.011	journal	July 2012
Biosynthesis of Nonribosomal Peptides Finking, Robert; Marahiel, Mohamed A. Annual Review of Microbiology, Vol. 58, Issue 1, p. 453-488 https://doi.org/10.1146/annurev.micro.58.030603.123615	journal	October 2004
Fungal volatile compounds induce production of the secondary metabolite Sodorifen in Serratia plymuthica PRI-2C Schmidt, Ruth; Jager, Victor de; Zühlke, Daniela Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-00893-3	journal	April 2017
Interactive Tree Of Life (iTOL) v4: recent updates and new developments Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz239	journal	April 2019
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13219	journal	October 2016
Macroecological patterns in soil communities: Soil community macroecology Decaëns, Thibaud Global Ecology and Biogeography, Vol. 19, Issue 3 https://doi.org/10.1111/j.1466-8238.2009.00517.x	journal	February 2010
Combinatorial biosynthesis of polyketides—a perspective Wong, Fong T.; Khosla, Chaitan Current Opinion in Chemical Biology, Vol. 16, Issue 1-2 https://doi.org/10.1016/j.cbpa.2012.01.018	journal	April 2012
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014

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59 BASIC BIOLOGICAL SCIENCES
metagenomics
secondary metabolism
soil microbiology

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