Vitamin interdependencies predicted by metagenomics-informed network analyses and validated in microbial community microcosms

Hessler, Tomas; Huddy, Robert J.; Sachdeva, Rohan; Lei, Shufei; Harrison, Susan T. L.; Diamond, Spencer; Banfield, Jillian F.

doi:10.1038/s41467-023-40360-4

Title: Vitamin interdependencies predicted by metagenomics-informed network analyses and validated in microbial community microcosms

Journal Article · 07 August 2023 · Nature Communications

DOI: https://doi.org/10.1038/s41467-023-40360-4 · OSTI ID:1994217

Hessler, Tomas;

; Sachdeva, Rohan;

;

Abstract Metagenomic or metabarcoding data are often used to predict microbial interactions in complex communities, but these predictions are rarely explored experimentally. Here, we use an organism abundance correlation network to investigate factors that control community organization in mine tailings-derived laboratory microbial consortia grown under dozens of conditions. The network is overlaid with metagenomic information about functional capacities to generate testable hypotheses. We develop a metric to predict the importance of each node within its local network environments relative to correlated vitamin auxotrophs, and predict that a Variovorax species is a hub as an important source of thiamine. Quantification of thiamine during the growth of Variovorax in minimal media show high levels of thiamine production, up to 100 mg/L. A few of the correlated thiamine auxotrophs are predicted to produce pantothenate, which we show is required for growth of Variovorax , supporting that a subset of vitamin-dependent interactions are mutualistic. A Cryptococcus yeast produces the B-vitamin pantothenate, and co-culturing with Variovorax leads to a 90-130-fold fitness increase for both organisms. Our study demonstrates the predictive power of metagenome-informed, microbial consortia-based network analyses for identifying microbial interactions that underpin the structure and functioning of microbial communities.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

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

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1994217

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 14; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (52)

Genome-resolved metagenomics of a bioremediation system for degradation of thiocyanate in mine water containing suspended solid tailings Rahman, Sumayah F.; Kantor, Rose S.; Huddy, Robert MicrobiologyOpen, Vol. 6, Issue 3 https://doi.org/10.1002/mbo3.446	journal	February 2017
Thiamin biosynthesis in prokaryotes Begley, T. P.; Downs, Diana M.; Ealick, Steven E. Archives of Microbiology, Vol. 171, Issue 5 https://doi.org/10.1007/s002030050713	journal	April 1999
Rapid Inference of Direct Interactions in Large-Scale Ecological Networks from Heterogeneous Microbial Sequencing Data Tackmann, Janko; Matias Rodrigues, João Frederico; von Mering, Christian Cell Systems, Vol. 9, Issue 3 https://doi.org/10.1016/j.cels.2019.08.002	journal	September 2019
Assembling stable syntrophic Escherichia coli communities by comprehensively identifying beneficiaries of secreted goods Noto Guillen, Mariana; Rosener, Brittany; Sayin, Serkan Cell Systems, Vol. 12, Issue 11 https://doi.org/10.1016/j.cels.2021.08.002	journal	November 2021
Network analysis methods for studying microbial communities: A mini review Matchado, Monica Steffi; Lauber, Michael; Reitmeier, Sandra Computational and Structural Biotechnology Journal, Vol. 19 https://doi.org/10.1016/j.csbj.2021.05.001	journal	January 2021
Construction of a thiamine pyrophosphate high-producing strain of Aspergillus oryzae by overexpression of three genes involved in thiamine biosynthesis Tokui, Misato; Kubodera, Takafumi; Gomi, Katsuya Journal of Bioscience and Bioengineering, Vol. 111, Issue 4 https://doi.org/10.1016/j.jbiosc.2010.12.011	journal	April 2011
Towards a deeper understanding of microbial communities: integrating experimental data with dynamic models Qian, Yili; Lan, Freeman; Venturelli, Ophelia S. Current Opinion in Microbiology, Vol. 62 https://doi.org/10.1016/j.mib.2021.05.003	journal	August 2021
Network thinking in ecology and evolution Proulx, S.; Promislow, D.; Phillips, P. Trends in Ecology & Evolution, Vol. 20, Issue 6 https://doi.org/10.1016/j.tree.2005.04.004	journal	June 2005
Integration of Biomass Formulations of Genome-Scale Metabolic Models with Experimental Data Reveals Universally Essential Cofactors in Prokaryotes Xavier, Joana C.; Patil, Kiran Raosaheb; Rocha, Isabel Metabolic Engineering, Vol. 39 https://doi.org/10.1016/j.ymben.2016.12.002	journal	January 2017
Improved biotin, thiamine, and lipoic acid biosynthesis by engineering the global regulator IscR Bali, Anne P.; Lennox-Hvenekilde, David; Myling-Petersen, Nils Metabolic Engineering, Vol. 60 https://doi.org/10.1016/j.ymben.2020.03.005	journal	July 2020
Genome-Resolved Meta-Omics Ties Microbial Dynamics to Process Performance in Biotechnology for Thiocyanate Degradation Kantor, Rose S.; Huddy, Robert J.; Iyer, Ramsunder Environmental Science & Technology, Vol. 51, Issue 5 https://doi.org/10.1021/acs.est.6b04477	journal	February 2017
Structural Studies of Thiamin Monophosphate Kinase in Complex with Substrates and Products ^† ^, ^‡ McCulloch, Kathryn M.; Kinsland, Cynthia; Begley, Tadhg P. Biochemistry, Vol. 47, Issue 12 https://doi.org/10.1021/bi800041h	journal	March 2008
Thiamine Pyrophosphate, a Coenzyme of Transketolase Racker, E.; Haba, G. De La; Leder, I. G. Journal of the American Chemical Society, Vol. 75, Issue 4 https://doi.org/10.1021/ja01100a526	journal	February 1953
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
Competitive and cooperative metabolic interactions in bacterial communities Freilich, Shiri; Zarecki, Raphy; Eilam, Omer Nature Communications, Vol. 2, Issue 1 https://doi.org/10.1038/ncomms1597	journal	September 2011
Uneven distribution of cobamide biosynthesis and dependence in bacteria predicted by comparative genomics Shelton, Amanda N.; Seth, Erica C.; Mok, Kenny C. The ISME Journal, Vol. 13, Issue 3 https://doi.org/10.1038/s41396-018-0304-9	journal	November 2018
Cocultivation of an ultrasmall environmental parasitic bacterium with lytic ability against bacteria associated with wastewater foams Batinovic, Steven; Rose, Jayson J. A.; Ratcliffe, Julian Nature Microbiology, Vol. 6, Issue 6 https://doi.org/10.1038/s41564-021-00892-1	journal	April 2021
Keystone taxa as drivers of microbiome structure and functioning Banerjee, Samiran; Schlaeppi, Klaus; van der Heijden, Marcel G. A. Nature Reviews Microbiology, Vol. 16, Issue 9 https://doi.org/10.1038/s41579-018-0024-1	journal	May 2018
A single bacterial genus maintains root growth in a complex microbiome Finkel, Omri M.; Salas-González, Isai; Castrillo, Gabriel Nature, Vol. 587, Issue 7832 https://doi.org/10.1038/s41586-020-2778-7	journal	September 2020
Targeted isolation and cultivation of uncultivated bacteria by reverse genomics Cross, Karissa L.; Campbell, James H.; Balachandran, Manasi Nature Biotechnology, Vol. 37, Issue 11 https://doi.org/10.1038/s41587-019-0260-6	journal	September 2019
A metabolic modeling platform for the computation of microbial ecosystems in time and space (COMETS) Dukovski, Ilija; Bajić, Djordje; Chacón, Jeremy M. Nature Protocols, Vol. 16, Issue 11 https://doi.org/10.1038/s41596-021-00593-3	journal	October 2021
Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle He, Xuesong; McLean, Jeffrey S.; Edlund, Anna Proceedings of the National Academy of Sciences, Vol. 112, Issue 1 https://doi.org/10.1073/pnas.1419038112	journal	December 2014
Comparative Genomics of the Vitamin B ₁₂ Metabolism and Regulation in Prokaryotes Rodionov, Dmitry A.; Vitreschak, Alexey G.; Mironov, Andrey A. Journal of Biological Chemistry, Vol. 278, Issue 42 https://doi.org/10.1074/jbc.M305837200	journal	July 2003
Isolation and cultivation of candidate phyla radiation Saccharibacteria (TM7) bacteria in coculture with bacterial hosts Murugkar, Pallavi P.; Collins, Andrew J.; Chen, Tsute Journal of Oral Microbiology, Vol. 12, Issue 1 https://doi.org/10.1080/20002297.2020.1814666	journal	January 2020
Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation Letunic, I.; Bork, P. Bioinformatics, Vol. 23, Issue 1 https://doi.org/10.1093/bioinformatics/btl529	journal	October 2006
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
FastSpar: rapid and scalable correlation estimation for compositional data Watts, Stephen C.; Ritchie, Scott C.; Inouye, Michael Bioinformatics, Vol. 35, Issue 6 https://doi.org/10.1093/bioinformatics/bty734	journal	August 2018
GToTree: a user-friendly workflow for phylogenomics Lee, Michael D. Bioinformatics, Vol. 35, Issue 20 https://doi.org/10.1093/bioinformatics/btz188	journal	March 2019
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
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
GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy Parks, Donovan H.; Chuvochina, Maria; Rinke, Christian Nucleic Acids Research, Vol. 50, Issue D1 https://doi.org/10.1093/nar/gkab776	journal	September 2021
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
Bioreactor microbial ecosystems for thiocyanate and cyanide degradation unravelled with genome-resolved metagenomics: Metagenomics of thiocyanate/cyanide biodegradation Kantor, Rose S.; van Zyl, A. Wynand; van Hille, Robert P. Environmental Microbiology, Vol. 17, Issue 12 https://doi.org/10.1111/1462-2920.12936	journal	July 2015
Serobactins-mediated iron acquisition systems optimize competitive fitness of H erbaspirillum seropedicae inside rice plants: Siderophores role in plant-endophyte interaction Rosconi, Federico; Trovero, María F.; de Souza, Emanuel M. Environmental Microbiology, Vol. 18, Issue 8 https://doi.org/10.1111/1462-2920.13202	journal	February 2016
‘Omics‐guided prediction of the pathway for metabolism of isoprene by Variovorax sp. WS11 Dawson, Robin A.; Rix, Gregory D.; Crombie, Andrew T. Environmental Microbiology, Vol. 24, Issue 11 https://doi.org/10.1111/1462-2920.16149	journal	August 2022
Sharing vitamins: Cobamides unveil microbial interactions Sokolovskaya, Olga M.; Shelton, Amanda N.; Taga, Michiko E. Science, Vol. 369, Issue 6499 https://doi.org/10.1126/science.aba0165	journal	July 2020
Synergistic Degradation of Linuron by a Bacterial Consortium and Isolation of a Single Linuron-Degrading Variovorax Strain Dejonghe, W.; Berteloot, E.; Goris, J. Applied and Environmental Microbiology, Vol. 69, Issue 3 https://doi.org/10.1128/AEM.69.3.1532-1541.2003	journal	March 2003
Isolation and Characterization of New Thiamine-Deregulated Mutants of Bacillus subtilis Schyns, G.; Potot, S.; Geng, Y. Journal of Bacteriology, Vol. 187, Issue 23 https://doi.org/10.1128/JB.187.23.8127-8136.2005	journal	November 2005
A mutation in Escherichia coli K-12 results in a requirement for thiamine and a decrease in L-serine deaminase activity Newman, E. B.; Miller, B.; Colebrook, L. D. Journal of Bacteriology, Vol. 161, Issue 1 https://doi.org/10.1128/jb.161.1.272-276.1985	journal	January 1985
The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss Morris, J. Jeffrey; Lenski, Richard E.; Zinser, Erik R. mBio, Vol. 3, Issue 2 https://doi.org/10.1128/mBio.00036-12	journal	March 2012
Bacterial endophytes of the wildflowerCrocus albiflorusanalyzed by characterization of isolates and by a cultivation-independent approach Reiter, Birgit; Sessitsch, Angela Canadian Journal of Microbiology, Vol. 52, Issue 2 https://doi.org/10.1139/w05-109	journal	February 2006
Macromolecular Organization of Enzyme Systems Reed, L. J.; Cox, D. J. Annual Review of Biochemistry, Vol. 35, Issue 1 https://doi.org/10.1146/annurev.bi.35.070166.000421	journal	June 1966
Saccharibacteria (TM7) in the Human Oral Microbiome Bor, B.; Bedree, J. K.; Shi, W. Journal of Dental Research, Vol. 98, Issue 5 https://doi.org/10.1177/0022034519831671	journal	February 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
Earth microbial co-occurrence network reveals interconnection pattern across microbiomes Ma, Bin; Wang, Yiling; Ye, Shudi Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00857-2	journal	June 2020
Inferring Correlation Networks from Genomic Survey Data Friedman, Jonathan; Alm, Eric J. PLoS Computational Biology, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pcbi.1002687	journal	September 2012
Species abundance correlations carry limited information about microbial network interactions Pinto, Susanne; Benincà, Elisa; van Nes, Egbert H. PLOS Computational Biology, Vol. 18, Issue 9 https://doi.org/10.1371/journal.pcbi.1010491	journal	September 2022
Isolation of new Methanol-Utilizing Bacteria and its Thiamine-Requirement for Growths Kouno, Kageaki; Oki, Toshikazu; Nomura, Hideo The Journal of General and Applied Microbiology, Vol. 19, Issue 1 https://doi.org/10.2323/jgam.19.11	journal	January 1973
Thiocyanate and Organic Carbon Inputs Drive Convergent Selection for Specific Autotrophic Afipia and Thiobacillus Strains Within Complex Microbiomes Huddy, Robert J.; Sachdeva, Rohan; Kadzinga, Fadzai Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.643368	journal	April 2021
A Genomic Perspective Across Earth’s Microbiomes Reveals That Genome Size in Archaea and Bacteria Is Linked to Ecosystem Type and Trophic Strategy Rodríguez-Gijón, Alejandro; Nuy, Julia K.; Mehrshad, Maliheh Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.761869	journal	January 2022
Variovorax sp. Has an Optimum Cell Density to Fully Function as a Plant Growth Promoter Natsagdorj, Oyungerel; Sakamoto, Hisayo; Santiago, Dennis Microorganisms, Vol. 7, Issue 3 https://doi.org/10.3390/microorganisms7030082	journal	March 2019
The ACC-Deaminase Producing Bacterium Variovorax sp. CT7.15 as a Tool for Improving Calicotome villosa Nodulation and Growth in Arid Regions of Tunisia Bessadok, Khouloud; Navarro-Torre, Salvadora; Pajuelo, Eloísa Microorganisms, Vol. 8, Issue 4 https://doi.org/10.3390/microorganisms8040541	journal	April 2020

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