Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production

Cobalamin (vitamin B12) is a complex metabolite and essential cofactor required by many branches of life, including most eukaryotic phytoplankton. Algae and other cobalamin auxotrophs rely on environmental cobalamin supplied from a relatively small set of cobalamin-producing prokaryotic taxa. Althou...

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Main Authors:	Doxey, Andrew C, Kurtz, Daniel A, Lynch, Michael DJ, Sauder, Laura A, Neufeld, Josh D
Format:	Online
Language:	English
Published:	Nature Publishing Group 2015
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4303638/

id	pubmed-4303638
recordtype	oai_dc
spelling	pubmed-43036382015-02-04 Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production Doxey, Andrew C Kurtz, Daniel A Lynch, Michael DJ Sauder, Laura A Neufeld, Josh D Original Article Cobalamin (vitamin B12) is a complex metabolite and essential cofactor required by many branches of life, including most eukaryotic phytoplankton. Algae and other cobalamin auxotrophs rely on environmental cobalamin supplied from a relatively small set of cobalamin-producing prokaryotic taxa. Although several Bacteria have been implicated in cobalamin biosynthesis and associated with algal symbiosis, the involvement of Archaea in cobalamin production is poorly understood, especially with respect to the Thaumarchaeota. Based on the detection of cobalamin synthesis genes in available thaumarchaeotal genomes, we hypothesized that Thaumarchaeota, which are ubiquitous and abundant in aquatic environments, have an important role in cobalamin biosynthesis within global aquatic ecosystems. To test this hypothesis, we examined cobalamin synthesis genes across sequenced thaumarchaeotal genomes and 430 metagenomes from a diverse range of marine, freshwater and hypersaline environments. Our analysis demonstrates that all available thaumarchaeotal genomes possess cobalamin synthesis genes, predominantly from the anaerobic pathway, suggesting widespread genetic capacity for cobalamin synthesis. Furthermore, although bacterial cobalamin genes dominated most surface marine metagenomes, thaumarchaeotal cobalamin genes dominated metagenomes from polar marine environments, increased with depth in marine water columns, and displayed seasonality, with increased winter abundance observed in time-series datasets (e.g., L4 surface water in the English Channel). Our results also suggest niche partitioning between thaumarchaeotal and cyanobacterial ribosomal and cobalamin synthesis genes across all metagenomic datasets analyzed. These results provide strong evidence for specific biogeographical distributions of thaumarchaeotal cobalamin genes, expanding our understanding of the global biogeochemical roles played by Thaumarchaeota in aquatic environments. Nature Publishing Group 2015-02 2014-08-15 /pmc/articles/PMC4303638/ /pubmed/25126756 http://dx.doi.org/10.1038/ismej.2014.142 Text en Copyright © 2015 International Society for Microbial Ecology http://creativecommons.org/licenses/by/3.0/ This work is licensed under a Creative Commons Attribution 3.0 Unported License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Doxey, Andrew C Kurtz, Daniel A Lynch, Michael DJ Sauder, Laura A Neufeld, Josh D
spellingShingle	Doxey, Andrew C Kurtz, Daniel A Lynch, Michael DJ Sauder, Laura A Neufeld, Josh D Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production
author_facet	Doxey, Andrew C Kurtz, Daniel A Lynch, Michael DJ Sauder, Laura A Neufeld, Josh D
author_sort	Doxey, Andrew C
title	Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production
title_short	Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production
title_full	Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production
title_fullStr	Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production
title_full_unstemmed	Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production
title_sort	aquatic metagenomes implicate thaumarchaeota in global cobalamin production
description	Cobalamin (vitamin B12) is a complex metabolite and essential cofactor required by many branches of life, including most eukaryotic phytoplankton. Algae and other cobalamin auxotrophs rely on environmental cobalamin supplied from a relatively small set of cobalamin-producing prokaryotic taxa. Although several Bacteria have been implicated in cobalamin biosynthesis and associated with algal symbiosis, the involvement of Archaea in cobalamin production is poorly understood, especially with respect to the Thaumarchaeota. Based on the detection of cobalamin synthesis genes in available thaumarchaeotal genomes, we hypothesized that Thaumarchaeota, which are ubiquitous and abundant in aquatic environments, have an important role in cobalamin biosynthesis within global aquatic ecosystems. To test this hypothesis, we examined cobalamin synthesis genes across sequenced thaumarchaeotal genomes and 430 metagenomes from a diverse range of marine, freshwater and hypersaline environments. Our analysis demonstrates that all available thaumarchaeotal genomes possess cobalamin synthesis genes, predominantly from the anaerobic pathway, suggesting widespread genetic capacity for cobalamin synthesis. Furthermore, although bacterial cobalamin genes dominated most surface marine metagenomes, thaumarchaeotal cobalamin genes dominated metagenomes from polar marine environments, increased with depth in marine water columns, and displayed seasonality, with increased winter abundance observed in time-series datasets (e.g., L4 surface water in the English Channel). Our results also suggest niche partitioning between thaumarchaeotal and cyanobacterial ribosomal and cobalamin synthesis genes across all metagenomic datasets analyzed. These results provide strong evidence for specific biogeographical distributions of thaumarchaeotal cobalamin genes, expanding our understanding of the global biogeochemical roles played by Thaumarchaeota in aquatic environments.
publisher	Nature Publishing Group
publishDate	2015
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4303638/
_version_	1613179802202669056

Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production

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