Determining the factors that influence marine microbial growth and community structure are critical for the understanding of global carbon cycling. Since the early twentieth century, it has been known that B vitamins play an important role in phytoplankton community dynamics. Limited oceanic dissolved B vitamin distributions indicate that these important coenzymes are present at picomolar levels, which could be too low to support maximal phytoplankton growth, and vast regions of the ocean exist where they are undetectable. Despite their importance, particulate B vitamin concentrations of field microbial populations are unknown. Here we report B vitamin concentrations measured in both the particulate and dissolved fractions, including multiple biochemically relevant B vitamin congeners. We establish their spatial distributions spanning distinct biogeographic and oceanographic regimes in the Mediterranean Sea and the Eastern Atlantic Ocean and show that all congeners are present both dissolved in seawater and in suspended particles. We observe that B vitamins cooccur in patches defined by regional biogeographic and oceanographic features. Additionally, distinct patterns of congener relative abundance in the dissolved and particulate pools provide insight to biological and chemical cycling of these compounds between and within the dissolved and particulate pools. Finally, linear model results demonstrate that model fits of microbial assemblages are strongest when they include both inorganic nutrients and dissolved B vitamin concentrations. We believe that these findings represent an advance in our understanding of B vitamin oceanographic distributions and point to interesting hypotheses of their influence on marine microbial ecology.
Coenzymes are essential across all domains of life. B vitamins (B1‐thiamin, B2‐riboflavin, B3‐niacin, B5‐pantothenate, B6‐pyridoxine, B7‐biotin, and B12‐cobalamin) represent the largest class of coenzymes, which participate in a diverse set of reactions including C1‐rearrangements, DNA repair, electron transfer, and fatty acid synthesis. B vitamin structures range from simple to complex heterocycles, yet, despite this complexity, multiple lines of evidence exist for their ancient origins including abiotic synthesis under putative early Earth conditions and/or meteorite transport. Thus, some of these critical coenzymes likely preceded life on Earth. Some modern organisms can synthesize their own B vitamins de novo while others must either scavenge them from the environment or establish a symbiotic relationship with a B vitamin producer. B vitamin requirements are widespread in some of the most ancient metabolisms including all six carbon fixation pathways, sulfate reduction, sulfur disproportionation, methanogenesis, acetogenesis, and photosynthesis. Understanding modern metabolic B vitamin requirements is critical for understanding the evolutionary conditions of ancient metabolisms as well as the biogeochemical cycling of critical elements such as S, C, and O.
The flavins (including flavin mononucleotide [FMN] and riboflavin [RF]) are a class of organic compounds synthesized by organisms to assist in critical redox reactions. While known to be secreted extracellularly by some species in laboratory-based cultures, flavin concentrations are largely unreported in the natural environment. Here, we present pore water and water column profiles of extracellular flavins (FMN and RF) and two degradation products (lumiflavin and lumichrome) from a coastal marine basin in the Southern California Bight alongside ancillary geochemical and 16S rRNA microbial community data. Flavins were detectable at picomolar concentrations in the water column (93-300 pM FMN, 14-40 pM RF) and low nanomolar concentrations in pore waters (250-2070 pM FMN, 11-210 pM RF). Elevated pore water flavin concentrations displayed an increasing trend with sediment depth and were significantly correlated with the total dissolved Fe (negative) and Mn (positive) concentrations. Network analysis revealed a positive relationship between flavins and the relative abundance of Dehalococcoidia and the MSBL9 clade of Planctomycetes, indicating possible secretion by members of these lineages. These results suggest that flavins are a common component of the so-called shared extracellular metabolite pool, especially in anoxic marine sediments where they exist at physiologicallyrelevant concentrations for metal oxide reduction.
Desert varnish is a dark rock coating that forms in arid environments worldwide. It is highly and selectively enriched in manganese, the mechanism for which has been a long-standing geological mystery. We collected varnish samples from diverse sites across the western United States, examined them in petrographic thin section using microscale chemical imaging techniques, and investigated the associated microbial communities using 16S amplicon and shotgun metagenomic DNA sequencing. Our analyses described a material governed by sunlight, water, and manganese redox cycling that hosts an unusually aerobic microbial ecosystem characterized by a remarkable abundance of photosynthetic Cyanobacteria in the genus Chroococcidiopsis as the major autotrophic constituent. We then showed that diverse Cyanobacteria, including the relevant Chroococcidiopsis taxon, accumulate extraordinary amounts of intracellular manganese—over two orders of magnitude higher manganese content than other cells. The speciation of this manganese determined by advanced paramagnetic resonance techniques suggested that the Cyanobacteria use it as a catalytic antioxidant—a valuable adaptation for coping with the substantial oxidative stress present in this environment. Taken together, these results indicated that the manganese enrichment in varnish is related to its specific uptake and use by likely founding members of varnish microbial communities.
Mono Lake is a closed-basin, hypersaline, alkaline lake located in Eastern Sierra Nevada, California, that is dominated by microbial life. This unique ecosystem offers a natural laboratory for probing microbial community responses to environmental change. In 2017, a heavy snowpack and subsequent runoff led Mono Lake to transition from annually mixed (monomictic) to indefinitely stratified (meromic-
Vitamin B1, or thiamin, can limit primary productivity in marine environments, however the major marine environmental sources of this essential coenzyme remain largely unknown. Vitamin B1 can only be produced by organisms that possess its complete synthesis pathway, while other organisms meet their cellular B1 quota by scavenging the coenzyme from exogenous sources. Due to high bacterial cell density and diversity, marine sediments could represent some of the highest concentrations of putative B1 producers, yet these environments have received little attention as a possible source of B1 to the overlying water column. Here we report the first dissolved pore water profiles of B1 measured in cores collected in two consecutive years from Santa Monica Basin, CA. Vitamin B1 concentrations were fairly consistent between the two years ranging from 30 pM up to 770 pM. A consistent maximum at ~5 cm sediment depth covaried with dissolved concentrations of iron. Pore water concentrations were higher than water column levels and represented some of the highest known environmental concentrations of B1 measured to date, (over two times higher than maximum water column concentrations) suggesting increased rates of cellular production and release within the sediments. A one dimensional diffusion-transport model applied to the B1 profile was used to estimate a diffusive benthic flux of ~0.7 nmol m−2 d−1. This is an estimated flux across the sediment-water interface in a deep sea basin; if similar magnitude B-vitamin fluxes occur in shallow coastal waters, benthic input could prove to be a significant B1-source to the water column and may play an important role in supplying this organic growth factor to auxotrophic primary producers.
The removal of chemical species from seawater during the precipitation of authigenic minerals is difficult to constrain but may play a major role in the global biogeochemical cycles of some elements, including silicon (Si) and germanium (Ge). Here, we present Ge/Si, δ 74 Ge, and supporting chemical data of pore waters and core incubations at three continental margin sites in California and the Gulf of Mexico. We used these data to partition Ge release and uptake by the various allogenic (delivered via sedimentation) and authigenic (formed in situ) phases in these sediments. About half of the pore water Ge (δ 74 Ge pw = 1.3-2.4‰) is supplied by biogenic silica dissolution (δ 74 Ge ∼ 3‰), with the other half contributed by lithogenic particulates (δ 74 Ge ∼ 0.6‰). The highest Ge/Si (∼3µmol/mol) and lowest δ 74 Ge (1.3-1.9‰) are observed at the Fe redox horizon, suggesting a supply from detrital Ge-rich Fe oxides. The precipitation of authigenic phases (most likely aluminosilicate clays) in deeper sediments preferentially incorporates Ge over Si, resulting in low pore water Ge/Si (∼0.3µmol/mol). The lack of corresponding δ 74 Ge pw trend indicates negligible Ge isotope fractionation during this process. Ge fluxes measured via core incubations were variable and appeared strongly controlled by Fe redox behavior near the sediment-water interface. In some cases, reductive Fe oxide dissolution appeared to enhance the benthic Ge flux by over 100% and released fractionated low δ 74 Ge of ∼−0.7‰, resulting in overall benthic δ 74 Ge inc between-0.2 and 3.6‰, depending on Fe oxide contribution to Ge flux. We estimate that detrital inputs supply 12-31% of total dissolved Ge to continental margin pore fluids globally, resulting in an average pore water and benthic flux δ 74 Ge between 2.2 and 2.7‰. Assuming 10-60% of pore water Ge is captured by the authigenic aluminosilicate sink, the dissolved Ge flux to the ocean derived from terrigenous inputs should be roughly 2.5-6.6 Mmol/y, much higher than previously estimated. Our results imply that authigenic Si burial in continental margins should be in the range of 1-8 Tmol/y (best estimate 3.1 Tmol/y), sufficient to close the global marine Si budget.
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