Dark ocean archaeal and bacterial chemoautotrophs drive vitamin B1 production in oxygen minimum zones

Vitamin B1 (thiamine) is essential for all cells, yet many marine microbes cannot synthesize B1 <i>de novo.</i> Dissolved thiamine and its related chemical congeners (TRCs) concentrations are not well characterized beyond the surface ocean, where they are typically low. Here, we observed unexpected enrichment of TRCs in regions of low dissolved oxygen levels (9.4 < O<sub>2</sub> < 12.5 μmol kg<sup>-1</sup>) across vertical profiles in Monterey Bay and Pacific waters 145 km offshore (Station 67-70). TRC concentrations ranged from fM to pM, with 1.1 to 4.5 fold increases from near-surface waters to the mesopelagic Oxygen Minimum Zone (OMZ). Notably, at 67-70, dissolved B1 increased 3.5-fold within the mesopelagic OMZ. Paired metagenomic analysis suggests that chemoautotrophic ammonia-oxidizing Archaea (AOA) and Thioglobaceae, alongside nitrite-oxidizing <i>Nitrospina</i>, are important B1 producers in OMZs. Metagenome-assembled genomes indicate that <i>Nitrospina</i> may alternate between B1 biosynthesis and energy-preserving salvage pathways in synergy with co-occurring AOA. Re-analysis of metatranscriptomic reads from a previous study established Thioglobaceae can be dominant expressors of key <i>de novo</i> B1 biosynthesis genes in Monterey Bay. These findings suggest that deep ocean chemoautotrophs are B1 prototrophs in OMZs, analogous to photoautotrophs in the epipelagic ocean, and provide the foundation for B1 trafficking.

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Journal
ISME Communications
Published
2025-01-01
DOI
https://doi.org/10.1093/ismeco/ycaf077
Primary Topic
Microbial Community Ecology and Physiology
Type
article
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article

Dark ocean archaeal and bacterial chemoautotrophs drive vitamin B1 production in oxygen minimum zones

Fabian Wittmers, Christopher P. Suffridge, Stephen J. Giovannoni, Alexandra Z. Worden et al.
1 links
ISME Communications
Microbial Community Ecology and Physiology
article

Dark ocean archaeal and bacterial chemoautotrophs drive vitamin B1 production in oxygen minimum zones

Fabian Wittmers, Christopher P. Suffridge, Stephen J. Giovannoni, Alexandra Z. Worden, Kristin Bergauer, Sebastian Sudek
article en

Abstract

Vitamin B1 (thiamine) is essential for all cells, yet many marine microbes cannot synthesize B1 <i>de novo.</i> Dissolved thiamine and its related chemical congeners (TRCs) concentrations are not well characterized beyond the surface ocean, where they are typically low. Here, we observed unexpected enrichment of TRCs in regions of low dissolved oxygen levels (9.4 < O<sub>2</sub> < 12.5 μmol kg<sup>-1</sup>) across vertical profiles in Monterey Bay and Pacific waters 145 km offshore (Station 67-70). TRC concentrations ranged from fM to pM, with 1.1 to 4.5 fold increases from near-surface waters to the mesopelagic Oxygen Minimum Zone (OMZ). Notably, at 67-70, dissolved B1 increased 3.5-fold within the mesopelagic OMZ. Paired metagenomic analysis suggests that chemoautotrophic ammonia-oxidizing Archaea (AOA) and Thioglobaceae, alongside nitrite-oxidizing <i>Nitrospina</i>, are important B1 producers in OMZs. Metagenome-assembled genomes indicate that <i>Nitrospina</i> may alternate between B1 biosynthesis and energy-preserving salvage pathways in synergy with co-occurring AOA. Re-analysis of metatranscriptomic reads from a previous study established Thioglobaceae can be dominant expressors of key <i>de novo</i> B1 biosynthesis genes in Monterey Bay. These findings suggest that deep ocean chemoautotrophs are B1 prototrophs in OMZs, analogous to photoautotrophs in the epipelagic ocean, and provide the foundation for B1 trafficking.

ISME CommunicationsVol. 5(1)
Oregon State University (US), Monterey Bay Aquarium Research Institute (US), Marine Biological Laboratory (US), GEOMAR Helmholtz Centre for Ocean Research Kiel (DE), University of Chicago (US)
National Science Foundation
Life below water
Openalex Percentile: Top 88%
Microbial Community Ecology and Physiology
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