title: Cyanobacteria and Eukaryotic Algae Use Different Chemical Variants of Vitamin B12.
abstract: Eukaryotic microalgae and prokaryotic cyanobacteria are the major components of the phytoplankton. Determining factors that govern growth of these primary producers, and how they interact, is therefore essential to understanding aquatic ecosystem productivity. Over half of microalgal species representing marine and freshwater habitats require for growth the corrinoid cofactor B12, which is synthesized de novo only by certain prokaryotes, including the majority of cyanobacteria. There are several chemical variants of B12, which are not necessarily functionally interchangeable. Cobalamin, the form bioavailable to humans, has as its lower axial ligand 5,6-dimethylbenzimidazole (DMB). Here, we show that the abundant marine cyanobacterium Synechococcus synthesizes only pseudocobalamin, in which the lower axial ligand is adenine. Moreover, bioinformatic searches of over 100 sequenced cyanobacterial genomes for B12 biosynthesis genes, including those involved in nucleotide loop assembly, suggest this is the form synthesized by cyanobacteria more broadly. We further demonstrate that pseudocobalamin is several orders of magnitude less bioavailable than cobalamin to several B12-dependent microalgae representing diverse lineages. This indicates that the two major phytoplankton groups use a different B12 currency. However, in an intriguing twist, some microalgal species can use pseudocobalamin if DMB is provided, suggesting that they are able to remodel the cofactor, whereas Synechococcus cannot. This species-specific attribute implicates algal remodelers as novel and keystone players of the B12 cycle, transforming our perception of the dynamics and complexity of the flux of this nutrient in aquatic ecosystems.
authors.affiliation: Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK. Electronic address: katherine.helliwell@mba.ac.uk.
authors.forename: Katherine Emma
authors.initials: KE
authors.lastname: Helliwell
authors.affiliation: School of Biosciences, University of Kent, Kent CT2 7NJ, UK.
authors.forename: Andrew David
authors.initials: AD
authors.lastname: Lawrence
authors.affiliation: Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK; Institute of Pharmacy and Molecular Biotechnology, Ruprecht-Karls University Heidelberg, Im Neuenheimer Feld 364, 69120 Heidelberg, Germany.
authors.forename: Andre
authors.initials: A
authors.lastname: Holzer
authors.affiliation: Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK.
authors.forename: Ulrich Johan
authors.initials: UJ
authors.lastname: Kudahl
authors.affiliation: Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK.
authors.forename: Severin
authors.initials: S
authors.lastname: Sasso
authors.affiliation: Institute of Organic Chemistry and Centre of Molecular Biosciences, University of Innsbruck, Innrain 80/82, 6020 Innsbruck, Austria.
authors.forename: Bernhard
authors.initials: B
authors.lastname: Kräutler
authors.affiliation: School of Life Sciences, University of Warwick, Coventry CV4 7AL, UK.
authors.forename: David John
authors.initials: DJ
authors.lastname: Scanlan
authors.affiliation: School of Biosciences, University of Kent, Kent CT2 7NJ, UK.
authors.forename: Martin James
authors.initials: MJ
authors.lastname: Warren
authors.affiliation: Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK. Electronic address: as25@cam.ac.uk.
authors.forename: Alison Gail
authors.initials: AG
authors.lastname: Smith
mesh_terms: D001426:Bacterial Proteins / Q000378:metabolism; D019295:Computational Biology / Q000379:methods; D005618:Fresh Water / Q000382:microbiology*; D010839:Phytoplankton / Q000378:metabolism*; D046940:Synechococcus / Q000378:metabolism*; D014805:Vitamin B 12 / Q000737:chemistry* / Q000378:metabolism*
chemical_list: D001426:Bacterial Proteins; D014805:Vitamin B 12
keywords: algae; competition; cyanobacteria; nutrient cycling; phytoplankton; pseudocobalamin; vitamin B(12)