Exploring Vitamin B1 Cycling and Its Connections to the Microbial Community in the North Atlantic Ocean

Vitamin B1 (thiamin) is an essential coenzyme for all cells. Recent findings from experimental cell biology and genome surveys have shown that thiamin cycling by plankton is far more complex than was previously understood. Many plankton cells cannot produce thiamin (are auxotrophic) and obligately require an exogenous source of thiamin or one or more of 5 different thiamin-related compounds (TRCs). Despite this emerging evidence for the evolution among plankton of complex interactions related to thiamin, the influence of TRCs on plankton community structure and productivity are not understood. We report measurements of three dissolved TRCs 4-amino-5-aminomethyl-2-methylpyrimidine (AmMP), 5-(2-hydroxyethyl)-4-methyl-1,3-thiazole-2-carboxylic acid (cHET), and 4-methyl-5-thiazoleethanol (HET) that have never before been assayed in seawater. Here we characterize them alongside other TRCs that were measured previously [thiamin and 4-amino-5-hydroxymethyl-2-methylpyrimidine (HMP)], in depth profiles from a latitudinal transect in the north Atlantic in March 2018. TRC concentrations ranged from femptomolar to picomolar. Surface depletion relative to a maximum near the bottom of the euphotic zone and low concentrations at deeper depths were consistent features. Our observations suggest that when bacterial abundance and production are low, TRC concentrations approach a steady state where TRC production and consumption terms are balanced. Standing stocks of TRCs also appear to be positively correlated with bacterial production. However, near the period of peak biomass in the accumulation phase of a bloom we observed an inverse relationship between TRCs and bacterial production, coincident with an increased abundance of Flavobacteria that comparative genomics indicates could be vitamin B1 auxotrophs. While these observations suggest that the dissolved pool of TRCs is often at steady state, with TRC production and consumption balanced, our data suggests that bloom induced shifts in microbial community structure and activity may cause a decoupling between TRC production and consumption, leading to increased abundances of some populations of bacteria that are putatively vitamin B1 auxotrophs.

[1]  S. Giovannoni,et al.  Seasonality of the Microbial Community Composition in the North Atlantic , 2021, Frontiers in Marine Science.

[2]  C. Carlson,et al.  Net Community Production, Dissolved Organic Carbon Accumulation, and Vertical Export in the Western North Atlantic , 2020, Frontiers in Marine Science.

[3]  D. Siegel,et al.  Phytoplankton Community Composition Determined From Co-variability Among Phytoplankton Pigments From the NAAMES Field Campaign , 2020, Frontiers in Marine Science.

[4]  Alison P. Chase,et al.  Small phytoplankton dominate western North Atlantic biomass , 2020, The ISME Journal.

[5]  M. Long,et al.  Phytoplankton Phenology in the North Atlantic: Insights From Profiling Float Measurements , 2020, Frontiers in Marine Science.

[6]  Alison P. Chase,et al.  Phytoplankton Growth and Productivity in the Western North Atlantic: Observations of Regional Variability From the NAAMES Field Campaigns , 2020, Frontiers in Marine Science.

[7]  P. Gaube,et al.  Overview of (Sub)mesoscale Ocean Dynamics for the NAAMES Field Program , 2019, Front. Mar. Sci..

[8]  C. Carlson,et al.  Regulation of Low and High Nucleic Acid Fluorescent Heterotrophic Prokaryote Subpopulations and Links to Viral-Induced Mortality Within Natural Prokaryote-Virus Communities , 2019, Microbial Ecology.

[9]  C. Pedrós-Alió,et al.  Delineation of ecologically distinct units of marine Bacteroidetes in the Northwestern Mediterranean Sea , 2019, Molecular ecology.

[10]  R. Breaker,et al.  A bacterial riboswitch class for the thiamin precursor HMP-PP employs a terminator-embedded aptamer , 2019, eLife.

[11]  E. Boss,et al.  The North Atlantic Aerosol and Marine Ecosystem Study (NAAMES): Science Motive and Mission Overview , 2019, Front. Mar. Sci..

[12]  R. Breaker,et al.  Author response: A bacterial riboswitch class for the thiamin precursor HMP-PP employs a terminator-embedded aptamer , 2019 .

[13]  Anders F. Andersson,et al.  Prevalent reliance of bacterioplankton on exogenous vitamin B1 and precursor availability , 2018, Proceedings of the National Academy of Sciences.

[14]  J. Maupin-Furlow Vitamin B1 (Thiamine) Metabolism and Regulation in Archaea , 2018, B Group Vitamins - Current Uses and Perspectives.

[15]  J. Gasol,et al.  B Vitamins and Their Congeners as Potential Drivers of Microbial Community Composition in an Oligotrophic Marine Ecosystem , 2018, Journal of Geophysical Research: Biogeosciences.

[16]  B. Cairns,et al.  Observations of Aerosol‐Cloud Interactions During the North Atlantic Aerosol and Marine Ecosystem Study , 2018, Geophysical Research Letters.

[17]  Thomas D. Niehaus,et al.  Author Correction: Carboxythiazole is a key microbial nutrient currency and critical component of thiamin biosynthesis , 2018, Scientific Reports.

[18]  Desmond G Higgins,et al.  TPP riboswitch-dependent regulation of an ancient thiamin transporter in Candida , 2018, PLoS genetics.

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

[20]  D. Relman,et al.  Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data , 2017, Microbiome.

[21]  S. Giovannoni,et al.  Globally Important Haptophyte Algae Use Exogenous Pyrimidine Compounds More Efficiently than Thiamin , 2017, mBio.

[22]  E. Boss,et al.  Student's tutorial on bloom hypotheses in the context of phytoplankton annual cycles , 2017, Global change biology.

[23]  S. Giovannoni,et al.  SAR202 Genomes from the Dark Ocean Predict Pathways for the Oxidation of Recalcitrant Dissolved Organic Matter , 2017, mBio.

[24]  Hadley Wickham,et al.  ggplot2 - Elegant Graphics for Data Analysis (2nd Edition) , 2017 .

[25]  S. Sañudo-Wilhelmy,et al.  A New Analytical Method for Direct Measurement of Particulate and Dissolved B-vitamins and Their Congeners in Seawater , 2017, Front. Mar. Sci..

[26]  S. Giovannoni,et al.  Newly discovered deep-branching marine plastid lineages are numerically rare but globally distributed , 2017, Current Biology.

[27]  L. Gómez-Consarnau,et al.  Life's utilization of B vitamins on early Earth , 2017, Geobiology.

[28]  F. Azam,et al.  Use of plankton-derived vitamin B1 precursors, especially thiazole-related precursor, by key marine picoeukaryotic phytoplankton , 2016, The ISME Journal.

[29]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[30]  J. Fuhrman,et al.  Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom , 2016, Nature Microbiology.

[31]  S. Jaenicke,et al.  Proteorhodopsin light-enhanced growth linked to vitamin-B1 acquisition in marine Flavobacteria , 2015, The ISME Journal.

[32]  F. Chavez,et al.  Cyanobacterial distributions along a physico-chemical gradient in the Northeastern Pacific Ocean. , 2015, Environmental microbiology.

[33]  W. Berelson,et al.  Vitamin B1 in marine sediments: pore water concentration gradient drives benthic flux with potential biological implications , 2015, Front. Microbiol..

[34]  Jed A. Fuhrman,et al.  Marine microbial community dynamics and their ecological interpretation , 2015, Nature Reviews Microbiology.

[35]  F. Azam,et al.  Vitamin B1 ecophysiology of marine picoeukaryotic algae: Strain‐specific differences and a new role for bacteria in vitamin cycling , 2015 .

[36]  D. Stahl,et al.  Determination of four forms of vitamin B12 and other B vitamins in seawater by liquid chromatography/tandem mass spectrometry. , 2014, Rapid communications in mass spectrometry : RCM.

[37]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[38]  J. Fuhrman,et al.  Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years , 2014, The ISME Journal.

[39]  J. Archibald,et al.  Alternatives to vitamin B1 uptake revealed with discovery of riboswitches in multiple marine eukaryotic lineages , 2014, The ISME Journal.

[40]  S. Giovannoni,et al.  Discovery of a SAR11 growth requirement for thiamin’s pyrimidine precursor and its distribution in the Sargasso Sea , 2014, The ISME Journal.

[41]  C. Arnosti,et al.  Composition and enzymatic function of particle-associated and free-living bacteria: a coastal/offshore comparison , 2014, The ISME Journal.

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

[43]  E. Boss,et al.  Resurrecting the ecological underpinnings of ocean plankton blooms. , 2014, Annual review of marine science.

[44]  C. Gobler,et al.  Effect of vitamins B1 and B12 on bloom dynamics of the harmful brown tide alga, Aureococcus anophagefferens (Pelagophyceae) , 2013 .

[45]  J. Fuhrman,et al.  Temporal variability and coherence of euphotic zone bacterial communities over a decade in the Southern California Bight , 2013, The ISME Journal.

[46]  Susan Holmes,et al.  phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data , 2013, PloS one.

[47]  S. Giovannoni,et al.  High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences , 2013, The ISME Journal.

[48]  C. Gobler,et al.  Vitamin B1 and B12 Uptake and Cycling by Plankton Communities in Coastal Ecosystems , 2012, Front. Microbio..

[49]  D. Karl,et al.  Multiple B-vitamin depletion in large areas of the coastal ocean , 2012, Proceedings of the National Academy of Sciences.

[50]  R. Amann,et al.  Substrate-Controlled Succession of Marine Bacterioplankton Populations Induced by a Phytoplankton Bloom , 2012, Science.

[51]  Richard Sanders,et al.  Export and mesopelagic particle flux during a North Atlantic spring diatom bloom , 2011 .

[52]  C. Gobler,et al.  Most harmful algal bloom species are vitamin B1 and B12 auxotrophs , 2010, Proceedings of the National Academy of Sciences.

[53]  T. Begley,et al.  The structural and biochemical foundations of thiamin biosynthesis. , 2009, Annual review of biochemistry.

[54]  B. Palenik,et al.  Temporal variation of Synechococcus clades at a coastal Pacific Ocean monitoring site , 2009, The ISME Journal.

[55]  Michael E Webb,et al.  Thiamine biosynthesis in algae is regulated by riboswitches , 2007, Proceedings of the National Academy of Sciences.

[56]  R. Amann,et al.  High local and global diversity of Flavobacteria in marine plankton. , 2007, Environmental microbiology.

[57]  I. Hewson,et al.  Annually reoccurring bacterial communities are predictable from ocean conditions , 2006, Proceedings of the National Academy of Sciences.

[58]  A. Chatterjee,et al.  Thiamin biosynthesis in eukaryotes: characterization of the enzyme-bound product of thiazole synthase from Saccharomyces cerevisiae and its implications in thiazole biosynthesis. , 2006, Journal of the American Chemical Society.

[59]  R. Breaker,et al.  Regulation of bacterial gene expression by riboswitches. , 2005, Annual review of microbiology.

[60]  Jang-Cheon Cho,et al.  Temporal and spatial response of bacterioplankton lineages to annual convective overturn at the Bermuda Atlantic Time‐series Study site , 2005 .

[61]  S. Sañudo-Wilhelmy,et al.  Direct determination of vitamin B1 in seawater by solid‐phase extraction and high‐performance liquid chromatography quantification , 2005 .

[62]  Francesc Peters,et al.  Changes in Bacterioplankton Composition under Different Phytoplankton Regimens , 2004, Applied and Environmental Microbiology.

[63]  Robert C. Edgar,et al.  MUSCLE: a multiple sequence alignment method with reduced time and space complexity , 2004, BMC Bioinformatics.

[64]  D. Kirchman The ecology of Cytophaga-Flavobacteria in aquatic environments. , 2002, FEMS microbiology ecology.

[65]  Sean V. Taylor,et al.  Thiamin biosynthesis in prokaryotes , 1999, Archives of Microbiology.

[66]  S. Giovannoni,et al.  16S rRNA genes reveal stratified open ocean bacterioplankton populations related to the Green Non-Sulfur bacteria. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[67]  A. Carlucci,et al.  DETERMINATION OF VITAMIN B12, THIAMINE, AND BIOTIN IN LAKE TAHOE WATERS USING MODIFIED MARINE BIOASSAY TECHNIQUES1 , 1972 .

[68]  A. Carlucci,et al.  INFLUENCE OF TEMPERATURE AND SOLAR RADIATION ON PERSISTENCE OF VITAMIN B12, THIAMINE, AND BIOTIN IN SEAWATER 1 , 1969, Journal of phycology.

[69]  O. A. Roels,et al.  Temperature Dependent Destruction of Thiamine in SEAWATER1 , 1966 .

[70]  L. Provasoli,et al.  Nutrition of Algae , 1964 .

[71]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[72]  M. Rapała-Kozik Vitamin B1 (Thiamine): A Cofactor for Enzymes Involved in the Main Metabolic Pathways and an Environmental Stress Protectant , 2011 .

[73]  J. Strickland The Ecology of the plankton off La Jolla, California,: In the period April through September, 1967 , 1970 .

[74]  K. Coward,et al.  The determination of vitamin A. , 1930, The Biochemical journal.