Nowinski et al., 2019, Scientific Data

Microbial Metagenomes and Metatranscriptomes During a Coastal Phytoplankton Bloom

Brent Nowinski, Christa B. Smith, Courtney M. Thomas, Kaitlin Esson, Roman Marin III., Christina M. Preston, James M. Birch, Christopher A. Scholin, Marcel Huntemann, Alicia Clum, Brian Foster, Bryce Foster, Simon Roux, Krishnaveni Palaniappan, Neha Varghese, Supratim Mukherjee, T. B. K. Reddy, Chris Daum, Alex Copeland, I.-Min A. Chen, Natalia N. Ivanova, Nikos C. Kyrpides, Tijana Glavina del Rio, William B. Whitman, Ronald P. Kiene, Emiley A. Eloe-Fadrosh, and Mary Ann Moran 

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Dimethylsulfoniopropionate (DMSP) is an abundant organic sulfur metabolite produced by many phytoplankton species and degraded by bacteria via two distinct pathways with climate-relevant implications. We assessed the diversity and abundance of bacteria possessing these pathways in the context of phytoplankton community composition over a three-week time period spanning September – October, 2014 in Monterey Bay, CA. The dmdAgene from the DMSP demethylation pathway dominated the DMSP gene pool and was harbored mostly by members of the alphaproteobacterial SAR11 clade and secondarily by the Roseobacter group, particularly during the second half of the study. Novel members of the DMSP-degrading community emerged from dmdA sequences recovered from metagenome assemblies and single-cell sequencing, including largely uncharacterized Gammaproteobacteria and Alphaproteobacteria taxa. In the DMSP cleavage pathway, the SAR11 gene dddK was the most abundant early in the study, but was supplanted by dddP over time. SAR11 members, especially those harboring genes for both DMSP degradation pathways, had a strong positive relationship with the abundance of dinoflagellates, and DMSP-degrading Gammaproteobacteria co-occurred with haptophytes. This in situstudy of the drivers of DMSP fate in a coastal ecosystem demonstrates for the first time correlations between specific groups of bacterial DMSP degraders and phytoplankton taxa.

Landa et al., 2019, ISME Journal

Sulfur metabolites that facilitate oceanic phytoplankton–bacteria carbon flux

Marine Landa, Andrew S. Burns, Bryndan P. Durham, Kaitlin Esson, Brent Nowinski, Shalabh Sharma, Alexey Vorobev, Torben Nielsen, Ronald P. Kiene, and Mary Ann Moran 

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Unlike biologically available nitrogen and phosphorus, which are often at limiting concentrations in surface seawater, sulfur in the form of sulfate is plentiful and not considered to constrain marine microbial activity. Nonetheless, in a model system in which a marine bacterium obtains all of its carbon from co-cultured phytoplankton, bacterial gene expression suggests that at least seven dissolved organic sulfur (DOS) metabolites support bacterial heterotrophy. These labile exometabolites of marine dinoflagellates and diatoms include taurine, N-acetyltaurine, isethionate, choline-O-sulfate, cysteate, 2,3-dihydroxypropane-1-sulfonate (DHPS), and dimethylsulfoniopropionate (DMSP). Leveraging from the compounds identified in this model system, we assessed the role of sulfur metabolites in the ocean carbon cycle by mining the Tara Oceans dataset for diagnostic genes. In the 1.4 million bacterial genome equivalents surveyed, estimates of the frequency of genomes harboring the capability for DOS metabolite utilization ranged broadly, from only 1 out of every 190 genomes (for the C2 sulfonate isethionate) to 1 out of every 5 (for the sulfonium compound DMSP). Bacteria able to participate in DOS transformations are dominated by Alphaproteobacteria in the surface ocean, but by SAR324, Acidimicrobiia, and Gammaproteobacteria at mesopelagic depths, where the capability for utilization occurs in higher frequency than in surface bacteria for more than half the sulfur metabolites. The discovery of an abundant and diverse suite of marine bacteria with the genetic capacity for DOS transformation argues for an important role for sulfur metabolites in the pelagic ocean carbon cycle.

Nowinski et al., 2019, Environmental Microbiology

Microdiversity and Temporal Dynamics of Marine Bacterial Dimethylsulfoniopropionate Genes

B. Nowinski, J. Motard-Côté, M. Landa, C. M. Preston, C. A. Scholin, J. M. Birch, R. P. Kiene, and M. A. Moran

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Dimethylsulfoniopropionate (DMSP) is an abundant organic sulfur metabolite produced by many phytoplankton species and degraded by bacteria via two distinct pathways with climate-relevant implications. We assessed the diversity and abundance of bacteria possessing these pathways in the context of phytoplankton community composition over a three-week time period spanning September – October, 2014 in Monterey Bay, CA. The dmdAgene from the DMSP demethylation pathway dominated the DMSP gene pool and was harbored mostly by members of the alphaproteobacterial SAR11 clade and secondarily by the Roseobacter group, particularly during the second half of the study. Novel members of the DMSP-degrading community emerged from dmdA sequences recovered from metagenome assemblies and single-cell sequencing, including largely uncharacterized Gammaproteobacteria and Alphaproteobacteria taxa. In the DMSP cleavage pathway, the SAR11 gene dddK was the most abundant early in the study, but was supplanted by dddP over time. SAR11 members, especially those harboring genes for both DMSP degradation pathways, had a strong positive relationship with the abundance of dinoflagellates, and DMSP-degrading Gammaproteobacteria co-occurred with haptophytes. This in situstudy of the drivers of DMSP fate in a coastal ecosystem demonstrates for the first time correlations between specific groups of bacterial DMSP degraders and phytoplankton taxa.

ISCA Sampling at Sapelo

Estelle Clerc visited us from the Stocker Lab (ETH, Switzerland) to conduct in situ chemotaxis assays at the UGA Marine Institute on Sapelo Island. In collaboration with Andrew Fu and Jeremy Schreier, Estelle collected data for her Ph.D. research on the key bacterial chemotaxis to marine phytoplankton exudates in marine ecosystems, including the identity of key metabolites and bacterial taxa involved.

Vorobev et al., 2018, Environmental Microbiology

Identifying Labile DOM Components in a Coastal Ocean through Depleted Bacterial Transcripts and Chemical Signals 

A. Vorobev, S. Sharma, M. Yu, J. Lee, B. J. Washington, W. B. Whitman, F. Ballantyne IV, P. M. Medeiros, and M. A. Moran

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Understanding which compounds comprising the complex and dynamic marine dissolved organic matter (DOM) pool are important in supporting heterotrophic bacterial production remains a major challenge. We eliminated sources of labile phytoplankton products, advected terrestrial material, and photodegradation products to coastal microbial communitiesby enclosing water samples in situ for 24 h in the dark. Bacterial genes for which expression decreased between the beginning and end of the incubationand chemical formulae that were depleted over this same time frame were usedas indicators of bioavailable compounds, an approach that avoids augmenting or modifying the natural DOM pool. Transport- and metabolism-related genes whose relative expression decreased implicated osmolytes, carboxylic acids, fatty acids, sugars, and organic sulfur compoundsas candidate bioreactive molecules. FT-ICR MS analysis of depleted molecular formulae implicated functional groups ~30-40 Da in size cleaved from semi-polar components of DOM as bioreactive components. Both gene expression and FT-ICR MS analyses indicated higher lability of compounds with sulfur and nitrogen heteroatoms. Untargeted methodologies able to integrate biological and chemical perspectives can be effective strategies for characterizing the labile microbial metabolites participating in carbon flux.

Gómez-Consarnau et al., 2018, Environmental Microbiology

Mosaic patterns of B‐vitamin synthesis and utilization in a natural marine microbial community

L. Gómez‐Consarnau, R. Sachdeva, S. M. Gifford, L. S. Cutter, J. A. Fuhrman, S. A. Sañudo‐Wilhelmy, M. A. Moran

Aquatic environments contain large communities of microorganisms whose synergistic interactions mediate the cycling of major and trace nutrients, including vitamins. B‐vitamins are essential coenzymes that many organisms cannot synthesize. Thus, their exchange among de novo synthesizers and auxotrophs is expected to play an important role in the microbial consortia and explain some of the temporal and spatial changes observed in diversity. In this study, we analyzed metatranscriptomes of a natural marine microbial community, diel sampled quarterly over one year to try to identify the potential major B‐vitamin synthesizers and consumers. Transcriptomic data showed that the best‐represented taxa dominated the expression of synthesis genes for some B‐vitamins but lacked transcripts for others. For instance, Rhodobacterales dominated the expression of vitamin‐B12 synthesis, but not of vitamin‐B7, whose synthesis transcripts were mainly represented by Flavobacteria. In contrast, bacterial groups that constituted less than 4% of the community (e.g., Verrucomicrobia) accounted for most of the vitamin‐B1 synthesis transcripts. Furthermore, ambient vitamin‐B1 concentrations were higher in samples collected during the day, and were positively correlated with chlorophyll‐a concentrations. Our analysis supports the hypothesis that the mosaic of metabolic interdependencies through B‐vitamin synthesis and exchange are key processes that contribute to shaping microbial communities in nature.