The diversity and ecological significance of microbial traits potentially involved in B12 biosynthesis in the global ocean

Cobalamin (B12), an essential nutrient and growth cofactor for many living organisms on the Earth, can be fully synthesized only by selected prokaryotes in nature. Therefore, microbial communities related with B12 biosynthesis could serve as an example subsystem to disentangle the underlying ecological mechanisms balancing the function and taxonomy of complex functional assemblages. By anchoring microbial traits potentially involved in B12 biosynthesis, we depict the biogeographic patterns of B12 biosynthesis genes and their carrying taxa in the global ocean, in light of the limitation to detect de novo B12 synthesizers via metagenomes alone. Both the taxonomic and functional composition of B12 biosynthesis genes were strongly shaped by depth, differentiating epipelagic from mesopelagic zones. The functional genes were relatively stably distributed across different oceans, but their carrying taxa varied considerably, showing clear functional redundancy of microbial systems. Microbial taxa carrying B12 biosynthesis genes in the surface water were influenced by environmental factors such as temperature, oxygen and nitrate. However, the composition of functional genes was weakly associated with these environmental factors. Null model analyses demonstrated that determinism governed the compositional variation of B12 biosynthesis genes, whereas a higher degree of stochasticity was associated with taxonomic variations. Significant associations were observed between chlorophyll a concentration and B12 biosynthesis traits, indicating their importance in global ocean primary production. Conclusively, this study revealed an essential ecological mechanism governing the assembly of microbes in nature: the environment selects function rather than taxonomy; functional redundancy underlies stochastic community assembly. Impact Statement A central question in ecology is how a galaxy of microbial taxa is assembled and distributed across space and through time, executing essential ecosystem functions. By anchoring microbial functional traits potentially involved in B12 biosynthesis and their carrying microbial taxa in the global ocean, this study addresses essential ecological questions from functional and taxonomic angles. Integrating multiple lines of evidence, we show that the ecosystem selects functional traits rather than taxonomic groups, and functional redundancy underlies stochastic taxonomic community assembly. Also, microbial communities potentially involved in B12 biosynthesis are significantly associated with chlorophyll a concentration, demonstrating their importance in global ocean primary production. This study provides valuable mechanistic insights into the complex microbial community assembly in natural ecosystems.

[1]  S. Sultana,et al.  Vitamin B12 is not shared by all marine prototrophic bacteria with their environment , 2023, The ISME journal.

[2]  Qichao Tu,et al.  To assemble or not to assemble: metagenomic profiling of microbially mediated biogeochemical pathways in complex communities , 2022, Briefings Bioinform..

[3]  M. Simon,et al.  Selection, drift and community interactions shape microbial biogeographic patterns in the Pacific Ocean , 2022, The ISME Journal.

[4]  Z. Khismatullina,et al.  Conflict of interest: the authors declare no conflict of interest. , 2021, Journal Biomed.

[5]  G. Cochrane,et al.  Tara Oceans: towards global ocean ecosystems biology , 2020, Nature Reviews Microbiology.

[6]  P. Nixon,et al.  Newly discovered Synechococcus sp. PCC 11901 is a robust cyanobacterial strain for high biomass production , 2020, Communications Biology.

[7]  R. Sommer,et al.  Bacterial vitamin B12 production enhances nematode predatory behavior , 2020, The ISME Journal.

[8]  S. Acinas,et al.  Disentangling the mechanisms shaping the surface ocean microbiota , 2019, Microbiome.

[9]  Luis Pedro Coelho,et al.  Gene Expression Changes and Community Turnover Differentially Shape the Global Ocean Metatranscriptome , 2019, Cell.

[10]  Jennifer Lu,et al.  Improved metagenomic analysis with Kraken 2 , 2019, Genome Biology.

[11]  A. Doxey,et al.  Metagenomic and chemical characterization of soil cobalamin production , 2019, The ISME Journal.

[12]  Jizhong Zhou,et al.  A general framework for quantitatively assessing ecological stochasticity , 2019, Proceedings of the National Academy of Sciences.

[13]  N. Fierer,et al.  High proportions of bacteria and archaea across most biomes remain uncultured , 2019, The ISME Journal.

[14]  Jizhong Zhou,et al.  Climate warming leads to divergent succession of grassland microbial communities , 2018, Nature Climate Change.

[15]  J. Fuhrman,et al.  Mosaic Patterns of B-vitamin Synthesis and Utilization in a Natural Marine Microbial Community , 2018, bioRxiv.

[16]  Erica C. Seth,et al.  Uneven distribution of cobamide biosynthesis and dependence in bacteria predicted by comparative genomics , 2018, The ISME Journal.

[17]  Michaeline B. N. Albright,et al.  Function and functional redundancy in microbial systems , 2018, Nature Ecology & Evolution.

[18]  E. Achterberg,et al.  Nutrient co-limitation at the boundary of an oceanic gyre , 2017, Nature.

[19]  Jizhong Zhou,et al.  Stochastic Community Assembly: Does It Matter in Microbial Ecology? , 2017, Microbiology and Molecular Biology Reviews.

[20]  C. Wheat,et al.  A dynamic microbial community with high functional redundancy inhabits the cold, oxic subseafloor aquifer , 2017, The ISME Journal.

[21]  T. Clauss,et al.  Elucidation of roles for vitamin B12 in regulation of folate, ubiquinone, and methionine metabolism , 2017, Proceedings of the National Academy of Sciences.

[22]  D. Stahl,et al.  Two distinct pools of B12 analogs reveal community interdependencies in the ocean , 2016, Proceedings of the National Academy of Sciences.

[23]  M. Doebeli,et al.  High taxonomic variability despite stable functional structure across microbial communities , 2016, Nature Ecology &Evolution.

[24]  M. Doebeli,et al.  Decoupling function and taxonomy in the global ocean microbiome , 2016, Science.

[25]  J. Lennon,et al.  Scaling laws predict global microbial diversity , 2016, Proceedings of the National Academy of Sciences.

[26]  B. Kräutler,et al.  Cyanobacteria and Eukaryotic Algae Use Different Chemical Variants of Vitamin B12 , 2016, Current Biology.

[27]  Tom O. Delmont,et al.  Phytoplankton–bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge , 2015, Proceedings of the National Academy of Sciences.

[28]  Luis Pedro Coelho,et al.  Structure and function of the global ocean microbiome , 2015, Science.

[29]  P. Bork,et al.  Tara Oceans studies plankton at planetary scale , 2015, Science.

[30]  S. Giovannoni,et al.  Rethinking the marine carbon cycle: Factoring in the multifarious lifestyles of microbes , 2015, Science.

[31]  Chao Xie,et al.  Fast and sensitive protein alignment using DIAMOND , 2014, Nature Methods.

[32]  P. Degnan,et al.  Vitamin B12 as a modulator of gut microbial ecology. , 2014, Cell metabolism.

[33]  A. Arkin,et al.  Stochasticity, succession, and environmental perturbations in a fluidic ecosystem , 2014, Proceedings of the National Academy of Sciences.

[34]  P. Degnan,et al.  Human gut microbes use multiple transporters to distinguish vitamin B₁₂ analogs and compete in the gut. , 2014, Cell host & microbe.

[35]  J. Sonnenburg,et al.  Gut microbes take their vitamins. , 2014, Cell host & microbe.

[36]  E. Webb,et al.  The role of B vitamins in marine biogeochemistry. , 2014, Annual review of marine science.

[37]  Jiajie Zhang,et al.  PEAR: a fast and accurate Illumina Paired-End reAd mergeR , 2013, Bioinform..

[38]  Mak A. Saito,et al.  Methionine synthase interreplacement in diatom cultures and communities: Implications for the persistence of B12 use by eukaryotic phytoplankton , 2013 .

[39]  A. Konopka,et al.  Quantifying community assembly processes and identifying features that impose them , 2013, The ISME Journal.

[40]  E. Bertrand,et al.  Influence of vitamin B auxotrophy on nitrogen metabolism in eukaryotic phytoplankton , 2012, Front. Microbio..

[41]  Charles F. F. Karney.  Algorithms for geodesics , 2011, Journal of Geodesy.

[42]  T. Thomas,et al.  Bacterial community assembly based on functional genes rather than species , 2011, Proceedings of the National Academy of Sciences.

[43]  Raymond E Goldstein,et al.  Insights into the evolution of vitamin B12 auxotrophy from sequenced algal genomes. , 2011, Molecular biology and evolution.

[44]  C. Gobler,et al.  The effect of vitamin B12 on phytoplankton growth and community structure in the Gulf of Alaska , 2011 .

[45]  Jonathan M. Chase,et al.  Using null models to disentangle variation in community dissimilarity from variation in α‐diversity , 2011 .

[46]  Fei-xue Fu,et al.  CO2 and vitamin B12 interactions determine bioactive trace metal requirements of a subarctic Pacific diatom , 2011, The ISME Journal.

[47]  David M. Karl,et al.  Vitamin B12 excretion by cultures of the marine cyanobacteria Crocosphaera and Synechococcus , 2010 .

[48]  J. Fuhrman.  General Distributions and the 'rare Biosphere' Microbial Community Structure and Its Functional Implications Review Insight , 2022 .

[49]  E. Delong,et al.  The Microbial Engines That Drive Earth's Biogeochemical Cycles , 2008, Science.

[50]  M. Saito,et al.  Vitamin B12 and iron colimitation of phytoplankton growth in the Ross Sea , 2007 .

[51]  C. Walsh,et al.  BluB cannibalizes flavin to form the lower ligand of vitamin B12 , 2007, Nature.

[52]  James H. Brown,et al.  Microbial biogeography: putting microorganisms on the map , 2006, Nature Reviews Microbiology.

[53]  Martin J. Warren,et al.  Algae acquire vitamin B12 through a symbiotic relationship with bacteria , 2005, Nature.

[54]  Helmut Hillebrand,et al.  On the Generality of the Latitudinal Diversity Gradient , 2004, The American Naturalist.

[55]  P. Dixon.  VEGAN, a package of R functions for community ecology , 2003 .

[56]  J. Escalante‐Semerena,et al.  The biosynthesis of adenosylcobalamin (vitamin B12). , 2002, Natural product reports.

[57]  K. Wilson,et al.  Vitamin B12: Insights into Biosynthesis's Mount Improbable , 1999 .

[58]  W. Whitman,et al.  Prokaryotes: the unseen majority. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[59]  J. Stubbe,et al.  Binding site revealed of nature's most beautiful cofactor. , 1994, Science.

[60]  R. Matthews,et al.  Comparison of cobalamin-independent and cobalamin-dependent methionine synthases from Escherichia coli: two solutions to the same chemical problem. , 1992, Biochemistry.

[61]  Jim Crawley,et al.  University of Oklahoma , 2019, The Grants Register 2022.

[62]  L. Breiman.  Random Forests , 2001, Machine Learning.

[63]  T. Bobik,et al.  Cobalamin (coenzyme B12): synthesis and biological significance. , 1996, Annual review of microbiology.

[64]  K. R. Clarke,et al.  A Method Of Linking Multivariate Community Structure To Environmental Variables , 1993 .

[65]  R. Aine.  of environmental variables , 1986 .