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1. Use and detection of a vitamin B1 degradation product yields new views of the marine B1 cycle and plankton metabolite exchange

   https://doi.org/10.1128/mbio.00061-23  

   Paerl, Ryan W; Curtis, Nathaniel P; Bittner, Meriel J; Cohn, Melanie R; Gifford, Scott M; Bannon, Catherine C; Rowland, Elden; Bertrand, Erin M (June 2023, mBio)

   Giovannoni, Stephen J (Ed.)

   ABSTRACT Vitamin B1 (thiamin) is a vital nutrient for most cells in nature, including marine plankton. Early and recent experiments show that B1 degradation products instead of B1 can support the growth of marine bacterioplankton and phytoplankton. However, the use and occurrence of some degradation products remains uninvestigated, namely N-formyl-4-amino-5-aminomethyl-2-methylpyrimidine (FAMP), which has been a focus of plant oxidative stress research. We investigated the relevance of FAMP in the ocean. Experiments and global ocean meta-omic data indicate that eukaryotic phytoplankton, including picoeukaryotes and harmful algal bloom species, use FAMP while bacterioplankton appear more likely to use deformylated FAMP, 4-amino-5-aminomethyl-2-methylpyrimidine. Measurements of FAMP in seawater and biomass revealed that it occurs at picomolar concentrations in the surface ocean, heterotrophic bacterial cultures produce FAMP in the dark—indicating non-photodegradation of B1 by cells, and B1-requiring (auxotrophic) picoeukaryotic phytoplankton produce intracellular FAMP. Our results require an expansion of thinking about vitamin degradation in the sea, but also the marine B1 cycle where it is now crucial to consider a new B1-related compound pool (FAMP), as well as generation (dark degradation—likely via oxidation), turnover (plankton uptake), and exchange of the compound within the networks of plankton. IMPORTANCEResults of this collaborative study newly show that a vitamin B1 degradation product, N-formyl-4-amino-5-aminomethyl-2-methylpyrimidine (FAMP), can be used by diverse marine microbes (bacteria and phytoplankton) to meet their vitamin B1 demands instead of B1 and that FAMP occurs in the surface ocean. FAMP has not yet been accounted for in the ocean and its use likely enables cells to avoid B1 growth deficiency. Additionally, we show FAMP is formed in and out of cells without solar irradiance—a commonly considered route of vitamin degradation in the sea and nature. Altogether, the results expand thinking about oceanic vitamin degradation, but also the marine B1 cycle where it is now crucial to consider a new B1-related compound pool (FAMP), as well as its generation (dark degradation—likely via oxidation), turnover (plankton uptake), and exchange within networks of plankton. 

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

   https://doi.org/10.3389/fmars.2020.606342  

   Suffridge, Christopher P.; Bolaños, Luis M.; Bergauer, Kristin; Worden, Alexandra Z.; Morré, Jeff; Behrenfeld, Michael J.; Giovannoni, Stephen J. (December 2020, Frontiers in Marine Science)

   null (Ed.)

   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. 

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3. Microbial transformation of virus-induced dissolved organic matter from picocyanobacteria: coupling of bacterial diversity and DOM chemodiversity

   https://doi.org/10.1038/s41396-019-0449-1  

   Zhao, Zhao; Gonsior, Michael; Schmitt-Kopplin, Philippe; Zhan, Yuanchao; Zhang, Rui; Jiao, Nianzhi; Chen, Feng (June 2019, The ISME Journal)

   Abstract Picocyanobacteria make up half of the ocean’s primary production, and they are subjected to frequent viral infection. Viral lysis of picocyanobacteria is a major driving force converting biologically fixed carbon into dissolved organic carbon (DOC). Viral-induced dissolved organic matter (vDOM) released from picocyanobacteria provides complex organic matter to bacterioplankton in the marine ecosystem. In order to understand how picocyanobacterial vDOM are transformed by bacteria and the impact of this process on bacterial community structure, viral lysate of picocyanobacteria was incubated with coastal seawater for 90 days. The transformation of vDOM was analyzed by ultrahigh-resolution mass spectrometry and the shift of bacterial populations analyzed using high-throughput sequencing technology. Addition of picocyanobacterial vDOM introduced abundant nitrogen components into the coastal water, which were largely degraded during the 90 days’ incubation period. However, some DOM signatures were accumulated and the total assigned formulae number increased over time. In contrast to the control (no addition of vDOM), bacterial community enriched with vDOM changed markedly with increased biodiversity indices. The network analysis showed that key bacterial species formed complex relationship with vDOM components, suggesting the potential correspondence between bacterial populations and DOM molecules. We demonstrate that coastal bacterioplankton are able to quickly utilize and transform lysis products of picocyanobacteria, meanwhile, bacterial community varies with changing chemodiverisity of DOM. vDOM released from picocyanobacteria generated a complex labile DOM pool, which was converted to a rather stable DOM pool after microbial processing in the time frame of days to weeks. 

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4. The Seasonal Flux and Fate of Dissolved Organic Carbon Through Bacterioplankton in the Western North Atlantic

   https://doi.org/10.3389/fmicb.2021.669883  

   Baetge, Nicholas; Behrenfeld, Michael J.; Fox, James; Halsey, Kimberly H.; Mojica, Kristina D.; Novoa, Anai; Stephens, Brandon M.; Carlson, Craig A. (June 2021, Frontiers in Microbiology)

   null (Ed.)

   The oceans teem with heterotrophic bacterioplankton that play an appreciable role in the uptake of dissolved organic carbon (DOC) derived from phytoplankton net primary production (NPP). As such, bacterioplankton carbon demand (BCD), or gross heterotrophic production, represents a major carbon pathway that influences the seasonal accumulation of DOC in the surface ocean and, subsequently, the potential vertical or horizontal export of seasonally accumulated DOC. Here, we examine the contributions of bacterioplankton and DOM to ecological and biogeochemical carbon flow pathways, including those of the microbial loop and the biological carbon pump, in the Western North Atlantic Ocean (∼39–54°N along ∼40°W) over a composite annual phytoplankton bloom cycle. Combining field observations with data collected from corresponding DOC remineralization experiments, we estimate the efficiency at which bacterioplankton utilize DOC, demonstrate seasonality in the fraction of NPP that supports BCD, and provide evidence for shifts in the bioavailability and persistence of the seasonally accumulated DOC. Our results indicate that while the portion of DOC flux through bacterioplankton relative to NPP increased as seasons transitioned from high to low productivity, there was a fraction of the DOM production that accumulated and persisted. This persistent DOM is potentially an important pool of organic carbon available for export to the deep ocean via convective mixing, thus representing an important export term of the biological carbon pump. 

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5. A global database of dissolved organic matter (DOM) concentration measurements in coastal waters (CoastDOM v1)

   https://doi.org/10.5194/essd-16-1107-2024  

   Lønborg, Christian; Carreira, Cátia; Abril, Gwenaël; Agustí, Susana; Amaral, Valentina; Andersson, Agneta; Arístegui, Javier; Bhadury, Punyasloke; Bif, Mariana B; Borges, Alberto V; et al (January 2024, Earth System Science Data)

   NA (Ed.)

   Abstract. Measurements of dissolved organic carbon (DOC), nitrogen (DON), and phosphorus (DOP) concentrations are used to characterize the dissolved organic matter (DOM) pool and are important components of biogeochemical cycling in the coastal ocean. Here, we present the first edition of a global database (CoastDOM v1; available at https://doi.org/10.1594/PANGAEA.964012, Lønborg et al., 2023) compiling previously published and unpublished measurements of DOC, DON, and DOP in coastal waters. These data are complemented by hydrographic data such as temperature and salinity and, to the extent possible, other biogeochemical variables (e.g. chlorophyll a, inorganic nutrients) and the inorganic carbon system (e.g. dissolved inorganic carbon and total alkalinity). Overall, CoastDOM v1 includes observations of concentrations from all continents. However, most data were collected in the Northern Hemisphere, with a clear gap in DOM measurements from the Southern Hemisphere. The data included were collected from 1978 to 2022 and consist of 62 338 data points for DOC, 20 356 for DON, and 13 533 for DOP. The number of measurements decreases progressively in the sequence DOC > DON > DOP, reflecting both differences in the maturity of the analytical methods and the greater focus on carbon cycling by the aquatic science community. The global database shows that the average DOC concentration in coastal waters (average ± standard deviation (SD): 182±314 µmol C L−1; median: 103 µmol C L−1) is 13-fold higher than the average coastal DON concentration (13.6±30.4 µmol N L−1; median: 8.0 µmol N L−1), which is itself 39-fold higher than the average coastal DOP concentration (0.34±1.11 µmol P L−1; median: 0.18 µmol P L−1). This dataset will be useful for identifying global spatial and temporal patterns in DOM and will help facilitate the reuse of DOC, DON, and DOP data in studies aimed at better characterizing local biogeochemical processes; closing nutrient budgets; estimating carbon, nitrogen, and phosphorous pools; and establishing a baseline for modelling future changes in coastal waters. 

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