Unprecedented DMSP Concentrations in a Massive Dinoflagellate Bloom in Monterey Bay, CA
Kiene, R. P., B. Nowinski, K. Esson, C. Preston, R. Marin III., J. Birch, C. Scholin, J. Ryan, and M. A. Moran
The organic sulfur compound dimethylsulfoniopropionate (DMSP) is synthesized by numerous species of marine phytoplankton, and its volatile degradation products are a major source of biogenic sulfur to the atmosphere. A massive bloom of the dinoflagellate Akashiwo sanguinea occurred in Monterey Bay, CA, USA,in the fall of 2016 and led to exceptionally high seawater DMSP concentrations that peaked at 4240 nM. Bacterial consumption rates showed that only a small fraction of the DMSP standing-stock flowed through the dissolved DMSP pool per day, contributing to the high DMSP concentrations and creating conditions conducive to production of dimethylsulfide (DMS). Conservative calculations of DMS yield from this persistent A. sanguinea bloom suggest substantial regional-scale inputs of DMS-sulfur to the atmosphere. Other recently reported major coastal blooms of A. sanguinea, along with indications that this species may benefit from climate change conditions, reveal a mechanism that could alter oceanic contributions to atmospheric sulfur pools.
Marine microbes play crucial roles in Earth’s element cycles through the production and consumption of organic matter. One of the elements whose fate is governed by microbial activities is sulfur, an essential constituent of biomass and a critical player in climate processes. Already well-studied in the ocean in its inorganic forms, organic sulfur compounds are now emerging as important chemical links between marine phytoplankton and bacteria. The high concentration of inorganic sulfur in seawater, which can be readily reduced by phytoplankton that are not limited for energy, provides an easy source of sulfur for biomolecule synthesis. Mechanisms such as exudation and cell lysis release these phytoplankton-derived sulfur metabolites into seawater, from which they are rapidly incorporated by marine bacteria and archaea. Energy-limited bacteria use scavenged sulfur metabolites as substrates or for the synthesis of vitamins, co-factors, signaling compounds, and antibiotics. Here we review current knowledge of the sulfur metabolites released into and taken up from the marine dissolved organic matter pool by microbial producers and consumers, and the ecological links facilitated by their diversity in structures, oxidation states, and chemistry.
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
Metagenomic and metatranscriptomic time-series data covering a 52-day period in the fall of 2016 provide an inventory of bacterial and archaeal community genes, transcripts, and taxonomy during an intense dinoflagellate bloom in Monterey Bay, CA, USA. The dataset comprises 84 metagenomes (0.8 terabases), 82 metatranscriptomes (1.1 terabases), and 88 16S rRNA amplicon libraries from samples collected on 41 dates. The dataset also includes 88 18S rRNA amplicon libraries, characterizing the taxonomy of the eukaryotic community during the bloom. Accompanying the sequence data are chemical and biological measurements associated with each sample. These datasets will facilitate studies of the structure and function of marine bacterial communities during episodic phytoplankton blooms.
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.
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 dmdA gene 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.
Estelle Clerc visited us from the Stocker Lab (ETH, Switzerland) to conduct insitu 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.
Jeremy Schreier, a doctoral student in the Department of Marine Sciences, studies microbial communities in the sunlit (euphotic) zone of the ocean environment. These microbial ecosystems contain diverse organisms connected by the exchange of metabolites (substances formed in or necessary for metabolism). Read more at the UGA web page…
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.
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.