Phylogenetic distribution and experimental characterization of corrinoid production and dependence in soil bacterial isolates

Alvarez-Aponte, Zoila I.; Govindaraju, Alekhya M.; Hallberg, Zachary F.; Nicolas, Alexa M.; Green, Myka A.; Mok, Kenny C.; Fonseca-García, Citlali; Coleman-Derr, Devin; Brodie, Eoin L.; Carlson, Hans K.; Taga, Michiko E.

doi:10.1093/ismejo/wrae068

Phylogenetic distribution and experimental characterization of corrinoid production and dependence in soil bacterial isolates

Journal Article · Mon Apr 22 00:00:00 EDT 2024 · The ISME Journal

DOI:https://doi.org/10.1093/ismejo/wrae068· OSTI ID:2407138

Alvarez-Aponte, Zoila I.; Govindaraju, Alekhya M.; Hallberg, Zachary F.; Nicolas, Alexa M.; Green, Myka A.; Mok, Kenny C.; Fonseca-García, Citlali; Coleman-Derr, Devin; Brodie, Eoin L.; Carlson, Hans K.; Taga, Michiko E.

Abstract

Soil microbial communities impact carbon sequestration and release, biogeochemical cycling, and agricultural yields. These global effects rely on metabolic interactions that modulate community composition and function. However, the physicochemical and taxonomic complexity of soil and the scarcity of available isolates for phenotypic testing are significant barriers to studying soil microbial interactions. Corrinoids—the vitamin B12 family of cofactors—are critical for microbial metabolism, yet they are synthesized by only a subset of microbiome members. Here, we evaluated corrinoid production and dependence in soil bacteria as a model to investigate the ecological roles of microorganisms involved in metabolic interactions. We isolated and characterized a taxonomically diverse collection of 161 soil bacteria from a single study site. Most corrinoid-dependent bacteria in the collection prefer B12 over other corrinoids, while all tested producers synthesize B12, indicating metabolic compatibility between producers and dependents in the collection. Furthermore, a subset of producers release B12 at levels sufficient to support dependent isolates in laboratory culture at estimated ratios of up to 1000 dependents per producer. Within our isolate collection, we did not find strong phylogenetic patterns in corrinoid production or dependence. Upon investigating trends in the phylogenetic dispersion of corrinoid metabolism categories across sequenced bacteria from various environments, we found that these traits are conserved in 47 out of 85 genera. Together, these phenotypic and genomic results provide evidence for corrinoid-based metabolic interactions among bacteria and provide a framework for the study of nutrient-sharing ecological interactions in microbial communities.

View Journal Article

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

Grant/Contract Number:: SC0020155

OSTI ID:: 2407138

Alternate ID(s):: OSTI ID: 2440631

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 1 Vol. 18; ISSN 1751-7362

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (70)

Microbial functional diversity: From concepts to applications Escalas, Arthur; Hale, Lauren; Voordeckers, James W. Ecology and Evolution, Vol. 9, Issue 20 https://doi.org/10.1002/ece3.5670	journal	September 2019
The role of soil microbes in the global carbon cycle: tracking the below-ground microbial processing of plant-derived carbon for manipulating carbon dynamics in agricultural systems: Role of soil microbes in global carbon cycle: carbon tracking & agro-cosystem management Gougoulias, Christos; Clark, Joanna M.; Shaw, Liz J. Journal of the Science of Food and Agriculture, Vol. 94, Issue 12 https://doi.org/10.1002/jsfa.6577	journal	March 2014
Strain dropouts reveal interactions that govern the metabolic output of the gut microbiome Wang, Min; Osborn, Lucas J.; Jain, Sunit Cell, Vol. 186, Issue 13 https://doi.org/10.1016/j.cell.2023.05.037	journal	June 2023
Mobilization of vitamin B12 transporters alters competitive dynamics in a human gut microbe Frye, Katie A.; Piamthai, Varadh; Hsiao, Ansel Cell Reports, Vol. 37, Issue 13 https://doi.org/10.1016/j.celrep.2021.110164	journal	December 2021
Cobamide Structure Depends on Both Lower Ligand Availability and CobT Substrate Specificity Crofts, Terence S.; Seth, Erica C.; Hazra, Amrita B. Chemistry & Biology, Vol. 20, Issue 10 https://doi.org/10.1016/j.chembiol.2013.08.006	journal	October 2013
Human Gut Microbes Use Multiple Transporters to Distinguish Vitamin B12 Analogs and Compete in the Gut Degnan, Patrick H.; Barry, Natasha A.; Mok, Kenny C. Cell Host & Microbe, Vol. 15, Issue 1 https://doi.org/10.1016/j.chom.2013.12.007	journal	January 2014
Cyanobacteria and Eukaryotic Algae Use Different Chemical Variants of Vitamin B12 Helliwell, Katherine Emma; Lawrence, Andrew David; Holzer, Andre Current Biology, Vol. 26, Issue 8 https://doi.org/10.1016/j.cub.2016.02.041	journal	April 2016
Belowground allocation and dynamics of recently fixed plant carbon in a California annual grassland Fossum, Christina; Estera-Molina, Katerina Y.; Yuan, Mengting Soil Biology and Biochemistry, Vol. 165 https://doi.org/10.1016/j.soilbio.2021.108519	journal	February 2022
Comparative Analysis of Corrinoid Profiles across Host-Associated and Environmental Samples Hallberg, Zachary F.; Seth, Erica C.; Thevasundaram, Kersh Biochemistry, Vol. 61, Issue 24 https://doi.org/10.1021/acs.biochem.2c00367	journal	August 2022
Vitamin B12 as a Growth Factor for Soil Bacteria Lochhead, A. G.; Thexton, R. H. Nature, Vol. 167, Issue 4260 https://doi.org/10.1038/1671034a0	journal	June 1951
Phylogenetic conservatism of functional traits in microorganisms Martiny, Adam C.; Treseder, Kathleen; Pusch, Gordon The ISME Journal, Vol. 7, Issue 4 https://doi.org/10.1038/ismej.2012.160	journal	December 2012
Fundamental shift in vitamin B12 eco-physiology of a model alga demonstrated by experimental evolution Helliwell, Katherine E.; Collins, Sinéad; Kazamia, Elena The ISME Journal, Vol. 9, Issue 6 https://doi.org/10.1038/ismej.2014.230	journal	December 2014
Algae acquire vitamin B12 through a symbiotic relationship with bacteria Croft, Martin T.; Lawrence, Andrew D.; Raux-Deery, Evelyne Nature, Vol. 438, Issue 7064 https://doi.org/10.1038/nature04056	journal	November 2005
A communal catalogue reveals Earth’s multiscale microbial diversity Thompson, Luke R.; Sanders, Jon G.; McDonald, Daniel Nature, Vol. 551, Issue 7681 https://doi.org/10.1038/nature24621	journal	November 2017
Exometabolite niche partitioning among sympatric soil bacteria Baran, Richard; Brodie, Eoin L.; Mayberry-Lewis, Jazmine Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9289	journal	September 2015
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
Metagenomic and chemical characterization of soil cobalamin production Lu, Xinda; Heal, Katherine R.; Ingalls, Anitra E. The ISME Journal, Vol. 14, Issue 1 https://doi.org/10.1038/s41396-019-0502-0	journal	September 2019
Vitamin B12 is not shared by all marine prototrophic bacteria with their environment Sultana, Sabiha; Bruns, Stefan; Wilkes, Heinz The ISME Journal, Vol. 17, Issue 6 https://doi.org/10.1038/s41396-023-01391-3	journal	March 2023
Bacteriophage-mediated lysis supports robust growth of amino acid auxotrophs Pherribo, Gordon J.; Taga, Michiko E. The ISME Journal, Vol. 17, Issue 10 https://doi.org/10.1038/s41396-023-01452-7	journal	June 2023
A subset of viruses thrives following microbial resuscitation during rewetting of a seasonally dry California grassland soil Nicolas, Alexa M.; Sieradzki, Ella T.; Pett-Ridge, Jennifer Nature Communications, Vol. 14, Issue 1 https://doi.org/10.1038/s41467-023-40835-4	journal	September 2023
Taxonomic and environmental distribution of bacterial amino acid auxotrophies Ramoneda, Josep; Jensen, Thomas B. N.; Price, Morgan N. Nature Communications, Vol. 14, Issue 1 https://doi.org/10.1038/s41467-023-43435-4	journal	November 2023
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao Nature Microbiology, Vol. 3, Issue 4 https://doi.org/10.1038/s41564-018-0129-3	journal	March 2018
The social network of microorganisms — how auxotrophies shape complex communities Zengler, Karsten; Zaramela, Livia S. Nature Reviews Microbiology, Vol. 16, Issue 6 https://doi.org/10.1038/s41579-018-0004-5	journal	March 2018
Soil microbiomes and one health Banerjee, Samiran; van der Heijden, Marcel G. A. Nature Reviews Microbiology, Vol. 21, Issue 1 https://doi.org/10.1038/s41579-022-00779-w	journal	August 2022
The predictive power of phylogeny on growth rates in soil bacterial communities Walkup, Jeth; Dang, Chansotheary; Mau, Rebecca L. ISME Communications, Vol. 3, Issue 1 https://doi.org/10.1038/s43705-023-00281-1	journal	July 2023
Geochemical constraints on bacteriophage infectivity in terrestrial environments Carlson, Hans K.; Piya, Denish; Moore, Madeline L. ISME Communications, Vol. 3, Issue 1 https://doi.org/10.1038/s43705-023-00297-7	journal	August 2023
Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys: Cultivation of soil bacteria Sait, Michelle; Hugenholtz, Philip; Janssen, Peter H. Environmental Microbiology, Vol. 4, Issue 11 https://doi.org/10.1046/j.1462-2920.2002.00352.x	journal	November 2002
Most harmful algal bloom species are vitamin B1 and B12 auxotrophs Tang, Y. Z.; Koch, F.; Gobler, C. J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 48 https://doi.org/10.1073/pnas.1009566107	journal	November 2010
Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice Goodman, A. L.; Kallstrom, G.; Faith, J. J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 15 https://doi.org/10.1073/pnas.1102938108	journal	March 2011
Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups Placella, S. A.; Brodie, E. L.; Firestone, M. K. Proceedings of the National Academy of Sciences, Vol. 109, Issue 27 https://doi.org/10.1073/pnas.1204306109	journal	June 2012
Two distinct pools of B ₁₂ analogs reveal community interdependencies in the ocean Heal, Katherine R.; Qin, Wei; Ribalet, Francois Proceedings of the National Academy of Sciences, Vol. 114, Issue 2 https://doi.org/10.1073/pnas.1608462114	journal	December 2016
Cell-to-cell bacterial interactions promoted by drier conditions on soil surfaces Tecon, Robin; Ebrahimi, Ali; Kleyer, Hannah Proceedings of the National Academy of Sciences, Vol. 115, Issue 39 https://doi.org/10.1073/pnas.1808274115	journal	September 2018
Microbiome interactions shape host fitness Gould, Alison L.; Zhang, Vivian; Lamberti, Lisa Proceedings of the National Academy of Sciences, Vol. 115, Issue 51 https://doi.org/10.1073/pnas.1809349115	journal	December 2018
SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes Pruesse, Elmar; Peplies, Jörg; Glöckner, Frank Oliver Bioinformatics, Vol. 28, Issue 14 https://doi.org/10.1093/bioinformatics/bts252	journal	May 2012
Decoding molecular interactions in microbial communities Abreu, Nicole A.; Taga, Michiko E. FEMS Microbiology Reviews, Vol. 40, Issue 5 https://doi.org/10.1093/femsre/fuw019	journal	July 2016
Biophysical processes supporting the diversity of microbial life in soil Tecon, Robin; Or, Dani FEMS Microbiology Reviews, Vol. 41, Issue 5 https://doi.org/10.1093/femsre/fux039	journal	August 2017
Soil microbial community response to corrinoids is shaped by a natural reservoir of vitamin B12 Hallberg, Zachary F.; Nicolas, Alexa M.; Alvarez-Aponte, Zoila I. The ISME Journal, Vol. 18, Issue 1 https://doi.org/10.1093/ismejo/wrae094	journal	January 2024
The RDP-II (Ribosomal Database Project) Maidak, B. L. Nucleic Acids Research, Vol. 29, Issue 1 https://doi.org/10.1093/nar/29.1.173	journal	January 2001
Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab301	journal	April 2021
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes Kim, M.; Oh, H. -S.; Park, S. -C. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 2 https://doi.org/10.1099/ijs.0.059774-0	journal	February 2014
The complete coenzyme B12 biosynthesis gene cluster of Lactobacillus reuteri CRL1098 Santos, Filipe; Vera, Jose L.; van der Heijden, René Microbiology, Vol. 154, Issue 1 https://doi.org/10.1099/mic.0.2007/011569-0	journal	January 2008
Identification of specific corrinoids reveals corrinoid modification in dechlorinating microbial communities: Corrinoids in dechlorinating communities Men, Yujie; Seth, Erica C.; Yi, Shan Environmental Microbiology, Vol. 17, Issue 12 https://doi.org/10.1111/1462-2920.12500	journal	June 2014
Less is More: Selective Advantages can Explain the Prevalent loss of Biosynthetic Genes in Bacteria: Adaptive loss of Biosynthetic Genes in Bacteria D'Souza, Glen; Waschina, Silvio; Pande, Samay Evolution, Vol. 68, Issue 9 https://doi.org/10.1111/evo.12468	journal	July 2014
Mutualistic interactions between vitamin B12-dependent algae and heterotrophic bacteria exhibit regulation: Algal-bacterial interactions for delivery of vitamin B12 Kazamia, Elena; Czesnick, Hjördis; Nguyen, Thi Thanh Van Environmental Microbiology, Vol. 14, Issue 6 https://doi.org/10.1111/j.1462-2920.2012.02733.x	journal	March 2012
A global atlas of the dominant bacteria found in soil Delgado-Baquerizo, Manuel; Oliverio, Angela M.; Brewer, Tess E. Science, Vol. 359, Issue 6373 https://doi.org/10.1126/science.aap9516	journal	January 2018
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
Unexpected Specificity of Interspecies Cobamide Transfer from Geobacter spp. to Organohalide-Respiring Dehalococcoides mccartyi Strains Yan, Jun; Ritalahti, Kirsti M.; Wagner, Darlene D. Applied and Environmental Microbiology, Vol. 78, Issue 18 https://doi.org/10.1128/AEM.01535-12	journal	July 2012
Thermotoga lettingae Can Salvage Cobinamide To Synthesize Vitamin B ₁₂ Butzin, Nicholas C.; Secinaro, Michael A.; Swithers, Kristen S. Applied and Environmental Microbiology, Vol. 79, Issue 22 https://doi.org/10.1128/AEM.01800-13	journal	September 2013
Versatility in Corrinoid Salvaging and Remodeling Pathways Supports Corrinoid-Dependent Metabolism in Dehalococcoides mccartyi Yi, Shan; Seth, Erica C.; Men, Yu-Jie Applied and Environmental Microbiology, Vol. 78, Issue 21 https://doi.org/10.1128/AEM.02150-12	journal	August 2012
Sustainable Growth of Dehalococcoides mccartyi 195 by Corrinoid Salvaging and Remodeling in Defined Lactate-Fermenting Consortia Men, Yujie; Seth, Erica C.; Yi, Shan Applied and Environmental Microbiology, Vol. 80, Issue 7 https://doi.org/10.1128/AEM.03477-13	journal	January 2014
Stimulation of Methanotrophic Growth in Cocultures by Cobalamin Excreted by Rhizobia Iguchi, Hiroyuki; Yurimoto, Hiroya; Sakai, Yasuyoshi Applied and Environmental Microbiology, Vol. 77, Issue 24 https://doi.org/10.1128/AEM.05834-11	journal	October 2011
Flexible Cobamide Metabolism in Clostridioides ( Clostridium ) difficile 630 Δ erm Shelton, Amanda N.; Lyu, Xun; Taga, Michiko E. Journal of Bacteriology, Vol. 202, Issue 2 https://doi.org/10.1128/JB.00584-19	journal	January 2020
Growth Inhibition of Sporomusa ovata by Incorporation of Benzimidazole Bases into Cobamides Mok, K. C.; Taga, M. E. Journal of Bacteriology, Vol. 195, Issue 9 https://doi.org/10.1128/JB.01282-12	journal	February 2013
Transport of Vitamin B ₁₂ in Escherichia coli Di Girolamo, Paula M.; Bradbeer, Clive Journal of Bacteriology, Vol. 106, Issue 3 https://doi.org/10.1128/jb.106.3.745-750.1971	journal	June 1971
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
Cofactor Selectivity in Methylmalonyl Coenzyme A Mutase, a Model Cobamide-Dependent Enzyme Sokolovskaya, Olga M.; Mok, Kenny C.; Park, Jong Duk mBio, Vol. 10, Issue 5 https://doi.org/10.1128/mBio.01303-19	journal	October 2019
Identification of a Novel Cobamide Remodeling Enzyme in the Beneficial Human Gut Bacterium Akkermansia muciniphila Mok, Kenny C.; Sokolovskaya, Olga M.; Nicolas, Alexa M. mBio, Vol. 11, Issue 6 https://doi.org/10.1128/mBio.02507-20	journal	December 2020
Stable-Isotope-Informed, Genome-Resolved Metagenomics Uncovers Potential Cross-Kingdom Interactions in Rhizosphere Soil Starr, Evan P.; Shi, Shengjing; Blazewicz, Steven J. mSphere, Vol. 6, Issue 5 https://doi.org/10.1128/mSphere.00085-21	journal	October 2021
Cobamide Sharing Is Predicted in the Human Skin Microbiome Swaney, Mary Hannah; Sandstrom, Shelby; Kalan, Lindsay R. mSystems, Vol. 7, Issue 5 https://doi.org/10.1128/msystems.00677-22	journal	October 2022
ON THE NATURE OF THE VITAMIN B₁₂ REQUIREMENT IN SOIL BACTERIA ISOLATED BY LOCHHEAD AND HIS CO-WORKERS Ford, J. E.; Hutner, S. H. Canadian Journal of Microbiology, Vol. 3, Issue 2 https://doi.org/10.1139/m57-036	journal	March 1957
Measurement of in Situ Activities of Nonphotosynthetic Microorganisms in Aquatic and Terrestrial Habitats Staley, J. T.; Konopka, A. Annual Review of Microbiology, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.mi.39.100185.001541	journal	October 1985
COBALAMIN (COENZYME B ₁₂ ): Synthesis and Biological Significance Roth, Jr; Lawrence, Jg; Bobik, Ta Annual Review of Microbiology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.micro.50.1.137	journal	October 1996
A 16S rDNA PCR-based theoretical to actual delta approach on culturable mock communities revealed severe losses of diversity information dos Santos, Hellen Ribeiro Martins; Argolo, Caio Suzart; Argôlo-Filho, Ronaldo Costa BMC Microbiology, Vol. 19, Issue 1 https://doi.org/10.1186/s12866-019-1446-2	journal	April 2019
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
Spatial Ecology of Bacteria at the Microscale in Soil Raynaud, Xavier; Nunan, Naoise PLoS ONE, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pone.0087217	journal	January 2014
Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes Magnúsdóttir, Stefanía; Ravcheev, Dmitry; de Crécy-Lagard, Valérie Frontiers in Genetics, Vol. 6 https://doi.org/10.3389/fgene.2015.00148	journal	April 2015
Bacterial Communities: Interactions to Scale Stubbendieck, Reed M.; Vargas-Bautista, Carol; Straight, Paul D. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01234	journal	August 2016
Micronutrient Requirements and Sharing Capabilities of the Human Gut Microbiome Rodionov, Dmitry A.; Arzamasov, Aleksandr A.; Khoroshkin, Matvei S. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01316	journal	June 2019
B-Vitamin Sharing Promotes Stability of Gut Microbial Communities Sharma, Vandana; Rodionov, Dmitry A.; Leyn, Semen A. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01485	journal	July 2019

Similar Records

Soil microbial community response to corrinoids is shaped by a natural reservoir of vitamin B12

Journal Article · Tue Jun 04 00:00:00 EDT 2024 · The ISME Journal · OSTI ID:2407196

Corrinoids as model nutrients to probe microbial interactions in a soil ecosystem

Technical Report · Thu Jan 11 23:00:00 EST 2024 · OSTI ID:2281020

Phylogenetic distribution and experimental characterization of corrinoid production and dependence in soil bacterial isolates

Citation Formats

References (70)

Similar Records

Related Subjects