Ligand cross-feeding resolves bacterial vitamin B12 auxotrophies

Cobalamin (vitamin B 12 , herein referred to as B 12 ) is an essential cofactor for most marine prokaryotes and eukaryotes 1 , 2 . Synthesized by a limited number of prokaryotes, its scarcity affects microbial interactions and community dynamics 2 – 4 . Here we show that two bacterial B 12 auxotroph...

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Published in:Nature (London) Vol. 629; no. 8013; pp. 886 - 892
Main Authors: Wienhausen, Gerrit, Moraru, Cristina, Bruns, Stefan, Tran, Den Quoc, Sultana, Sabiha, Wilkes, Heinz, Dlugosch, Leon, Azam, Farooq, Simon, Meinhard
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 23.05.2024
Nature Publishing Group
Subjects:
13/31
14/63
38/32
45/23
45/91
631/158/2463
631/326/2565/547
631/326/41/2535
631/45/320
64
Auxotrophs
Bacteria
Bioavailability
Biosynthesis
Cell culture
Consortia
Cyanocobalamin
Ecosystems
Genomes
Genomics
Humanities and Social Sciences
Ligands
Marine ecosystems
Metabolites
Microorganisms
multidisciplinary
Oceans
Plankton
Prokaryotes
Science
Science (multidisciplinary)
Syntrophism
Vitamin B12
ISSN:0028-0836, 1476-4687, 1476-4687
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Abstract Cobalamin (vitamin B 12 , herein referred to as B 12 ) is an essential cofactor for most marine prokaryotes and eukaryotes 1 , 2 . Synthesized by a limited number of prokaryotes, its scarcity affects microbial interactions and community dynamics 2 – 4 . Here we show that two bacterial B 12 auxotrophs can salvage different B 12 building blocks and cooperate to synthesize B 12 . A Colwellia sp. synthesizes and releases the activated lower ligand α-ribazole, which is used by another B 12 auxotroph, a Roseovarius sp., to produce the corrin ring and synthesize B 12 . Release of B 12 by Roseovarius sp. happens only in co-culture with Colwellia sp. and only coincidently with the induction of a prophage encoded in Roseovarius sp. Subsequent growth of Colwellia sp. in these conditions may be due to the provision of B 12 by lysed cells of Roseovarius sp. Further evidence is required to support a causative role for prophage induction in the release of B 12 . These complex microbial interactions of ligand cross-feeding and joint B 12 biosynthesis seem to be widespread in marine pelagic ecosystems. In the western and northern tropical Atlantic Ocean, bacteria predicted to be capable of salvaging cobinamide and synthesizing only the activated lower ligand outnumber B 12 producers. These findings add new players to our understanding of B 12 supply to auxotrophic microorganisms in the ocean and possibly in other ecosystems. Two species of auxotrophic marine bacteria are shown to share precursors to synthesize the essential cofactor vitamin B 12 , and such ligand cross-feeding may be a common phenomenon in the ocean and other ecosystems.
AbstractList Cobalamin (vitamin B 12 , herein referred to as B 12 ) is an essential cofactor for most marine prokaryotes and eukaryotes 1 , 2 . Synthesized by a limited number of prokaryotes, its scarcity affects microbial interactions and community dynamics 2 – 4 . Here we show that two bacterial B 12 auxotrophs can salvage different B 12 building blocks and cooperate to synthesize B 12 . A Colwellia sp. synthesizes and releases the activated lower ligand α-ribazole, which is used by another B 12 auxotroph, a Roseovarius sp., to produce the corrin ring and synthesize B 12 . Release of B 12 by Roseovarius sp. happens only in co-culture with Colwellia sp. and only coincidently with the induction of a prophage encoded in Roseovarius sp. Subsequent growth of Colwellia sp. in these conditions may be due to the provision of B 12 by lysed cells of Roseovarius sp. Further evidence is required to support a causative role for prophage induction in the release of B 12 . These complex microbial interactions of ligand cross-feeding and joint B 12 biosynthesis seem to be widespread in marine pelagic ecosystems. In the western and northern tropical Atlantic Ocean, bacteria predicted to be capable of salvaging cobinamide and synthesizing only the activated lower ligand outnumber B 12 producers. These findings add new players to our understanding of B 12 supply to auxotrophic microorganisms in the ocean and possibly in other ecosystems. Two species of auxotrophic marine bacteria are shown to share precursors to synthesize the essential cofactor vitamin B 12 , and such ligand cross-feeding may be a common phenomenon in the ocean and other ecosystems.
Cobalamin (vitamin B12, herein referred to as B12) is an essential cofactor for most marine prokaryotes and eukaryotes1,2. Synthesized by a limited number of prokaryotes, its scarcity affects microbial interactions and community dynamics2-4. Here we show that two bacterial B12 auxotrophs can salvage different B12 building blocks and cooperate to synthesize B12. A Colwellia sp. synthesizes and releases the activated lower ligand α-ribazole, which is used by another B12 auxotroph, a Roseovarius sp., to produce the corrin ring and synthesize B12. Release of B12 by Roseovarius sp. happens only in co-culture with Colwellia sp. and only coincidently with the induction of a prophage encoded in Roseovarius sp. Subsequent growth of Colwellia sp. in these conditions may be due to the provision of B12 by lysed cells of Roseovarius sp. Further evidence is required to support a causative role for prophage induction in the release of B12. These complex microbial interactions of ligand cross-feeding and joint B12 biosynthesis seem to be widespread in marine pelagic ecosystems. In the western and northern tropical Atlantic Ocean, bacteria predicted to be capable of salvaging cobinamide and synthesizing only the activated lower ligand outnumber B12 producers. These findings add new players to our understanding of B12 supply to auxotrophic microorganisms in the ocean and possibly in other ecosystems.Cobalamin (vitamin B12, herein referred to as B12) is an essential cofactor for most marine prokaryotes and eukaryotes1,2. Synthesized by a limited number of prokaryotes, its scarcity affects microbial interactions and community dynamics2-4. Here we show that two bacterial B12 auxotrophs can salvage different B12 building blocks and cooperate to synthesize B12. A Colwellia sp. synthesizes and releases the activated lower ligand α-ribazole, which is used by another B12 auxotroph, a Roseovarius sp., to produce the corrin ring and synthesize B12. Release of B12 by Roseovarius sp. happens only in co-culture with Colwellia sp. and only coincidently with the induction of a prophage encoded in Roseovarius sp. Subsequent growth of Colwellia sp. in these conditions may be due to the provision of B12 by lysed cells of Roseovarius sp. Further evidence is required to support a causative role for prophage induction in the release of B12. These complex microbial interactions of ligand cross-feeding and joint B12 biosynthesis seem to be widespread in marine pelagic ecosystems. In the western and northern tropical Atlantic Ocean, bacteria predicted to be capable of salvaging cobinamide and synthesizing only the activated lower ligand outnumber B12 producers. These findings add new players to our understanding of B12 supply to auxotrophic microorganisms in the ocean and possibly in other ecosystems.
Cobalamin (vitamin B12, herein referred to as B12) is an essential cofactor for most marine prokaryotes and eukaryotes1,2. Synthesized by a limited number of prokaryotes, its scarcity affects microbial interactions and community dynamics2 4. Here we show that two bacterial B12 auxotrophs can salvage different B12 building blocks and cooperate to synthesize B12. A Colivellia sp. synthesizes and releases the activated lower ligand a-ribazole, which is used by another B12 auxotroph, a Roseouarius sp., to produce the corrin ring and synthesize B12. Release of B12 by Roseouarius sp. happens only in co-culture with Colivellia sp. and only coincidently with the induction of a prophage encoded in Roseouarius sp. Subsequent growth of Colivellia sp. in these conditions may be due to the provision of B12 by lysed cells of Roseouarius sp. Further evidence is required to support a causative role for prophage induction in the release of B12. These complex microbial interactions of ligand cross-feeding and joint B12 biosynthesis seem to be widespread in marine pelagic ecosystems. In the western and northern tropical Atlantic Ocean, bacteria predicted to be capable of salvaging cobinamide and synthesizing only the activated lower ligand outnumber B12 producers. These findings add new players to our understanding of B12 supply to auxotrophic microorganisms in the ocean and possibly in other ecosystems.
Author Wienhausen, Gerrit
Sultana, Sabiha
Bruns, Stefan
Wilkes, Heinz
Azam, Farooq
Simon, Meinhard
Dlugosch, Leon
Moraru, Cristina
Tran, Den Quoc
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  organization: Institute for Chemistry and Biology of the Marine Environment (ICBM), School of Mathematics and Science, Carl von Ossietzky Universität Oldenburg, Scripps Institution of Oceanography, Marine Biology Research Division, University of California San Diego
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  surname: Moraru
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  organization: Institute for Chemistry and Biology of the Marine Environment (ICBM), School of Mathematics and Science, Carl von Ossietzky Universität Oldenburg, Environmental Metagenomics, Research Center One Health Ruhr of the University Alliance Ruhr, Faculty of Chemistry, University of Duisburg-Essen
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  email: meinhard.simon@uni-oldenburg.de
  organization: Institute for Chemistry and Biology of the Marine Environment (ICBM), School of Mathematics and Science, Carl von Ossietzky Universität Oldenburg, Helmholtz Institute for Functional Marine Biodiversity at the University of Oldenburg (HIFMB)
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Snippet Cobalamin (vitamin B 12 , herein referred to as B 12 ) is an essential cofactor for most marine prokaryotes and eukaryotes 1 , 2 . Synthesized by a limited...
Cobalamin (vitamin B12, herein referred to as B12) is an essential cofactor for most marine prokaryotes and eukaryotes1,2. Synthesized by a limited number of...
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Auxotrophs
Bacteria
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Cyanocobalamin
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Humanities and Social Sciences
Ligands
Marine ecosystems
Metabolites
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Plankton
Prokaryotes
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Science (multidisciplinary)
Syntrophism
Vitamin B12
Title Ligand cross-feeding resolves bacterial vitamin B12 auxotrophies
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