Nowinski and Moran, 2021, Nature Microbiology

Niche Dimensions of a Marine Bacterium are Identified Using Invasion Studies in Coastal Seawater

B. Nowinski, M. A. Moran

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Niche theory is a foundational ecological concept that explains the distribution of species in natural environments. Identifying the dimensions of any organism’s niche is challenging because numerous environmental factors can affect organism viability. We used serial invasion experiments to introduce Ruegeria pomeroyi DSS-3, a heterotrophic marine bacterium, into a coastal phytoplankton bloom on 14 dates. RNA-sequencing analysis of R. pomeroyi was conducted after 90 min to assess its niche dimensions in this dynamic ecosystem. We identified ~100 external conditions eliciting transcriptional responses, which included substrates, nutrients, metals and biotic interactions such as antagonism, resistance and cofactor synthesis. The peak bloom was characterized by favourable states for most of the substrate dimensions, but low inferred growth rates of R. pomeroyi at this stage indicated that its niche was narrowed by factors other than substrate availability, most probably negative biotic interactions with the bloom dinoflagellate. Our findings indicate chemical and biological features of the ocean environment that can constrain where heterotrophic bacteria survive.

Uchimiya et al., 2020, BioRXiv

Diel Investments in Phytoplankton Metabolic Production Influenced by Associated Heterotrophic Bacteria

M. Uchimiya, W. Schroer, M. Olofsson, A. S. Edison, M. A. Moran

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Organic carbon transfer between photoautotrophic and heterotrophic microbes in the surface ocean mediated through metabolites dissolved in seawater is a central but poorly understood process in the global carbon cycle. In a synthetic microbial community in which diatom extracellular release of organic molecules sustained growth of a co-cultured bacterium, metabolite transfer was assessed over two diel cycles based on per cell quantification of phytoplankton endometabolites and bacterial transcripts. Of 31 phytoplankton endometabolites identified and classified into temporal abundance patterns, eight could be matched to patterns of bacterial transcripts mediating their uptake and catabolism. A model simulating the coupled endometabolite-transcription relationships hypothesized that one category of outcomes required an increase in phytoplankton metabolite synthesis in response to the presence of the bacterium. An experimental test of this hypothesis confirmed higher endometabolome accumulation in the presence of bacteria for all five compounds assigned to this category – leucine, glycerol-3-phosphate, glucose, and the organic sulfur compounds dihydroxypropanesulfonate and dimethylsulfoniopropionate. Partitioning of photosynthate into rapidly-cycling dissolved organic molecules at the expense of phytoplankton biomass production has implications for carbon sequestration in the deep ocean. That heterotrophic bacteria can impact this partitioning suggests a previously unrecognized influence on the ocean’s carbon reservoirs. 

Ferrer-González et al., 2020, ISME Journal

Resource Partitioning of Phytoplankton Metabolites that Support Bacterial Heterotrophy

Ferrer-González, F. X.,  B. Widner, N. R. Holderman, J. Glushka, A. S. Edison, E. B. Kujawinski, and  M. A. Moran

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The communities of bacteria that assemble around marine microphytoplankton are predictably dominated by Rhodobacterales, Flavobacteriales, and families within the Gammaproteobacteria. Yet whether this consistent ecological pattern reflects the result of resource-based niche partitioning or resource competition requires better knowledge of the metabolites linking microbial autotrophs and heterotrophs in the surface ocean. We characterized molecules targeted for uptake by three heterotrophic bacteria individually co-cultured with a marine diatom using two strategies that vetted the exometabolite pool for biological relevance by means of bacterial activity assays: expression of diagnostic genes and net drawdown of exometabolites, the latter detected with mass spectrometry (MS) and nuclear magnetic resonance (NMR) using novel sample preparation approaches. Of the more than 36 organic molecules with evidence of bacterial uptake, 53% contained nitrogen (including nucleosides and amino acids), 11% were organic sulfur compounds (including dihydroxypropanesulfonate and dimethysulfoniopropionate), and 28% were components of polysaccharides (including chrysolaminarin, chitin, and alginate). Overlap in phytoplankton-derived metabolite use by bacteria in the absence of competition was low, and only guanosine, proline, and N-acetyl-D-glucosamine were predicted to be used by all three. Exometabolite uptake pattern points to a key role for ecological resource partitioning in the assembly marine bacterial communities transforming recent photosynthate.

Fu et al., 2020, Proceedings of the National Academy of Sciences

Ecological Drivers of Bacterial Community Assembly in Synthetic Phycospheres

Fu, H., M. Uchimiya, J. Gore, and M. A. Moran

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In the nutrient rich region surrounding marine phytoplankton cells, heterotrophic bacterioplankton transform a major fraction of recently fixed carbon through the uptake and catabolism of phytoplankton metabolites. We sought to understand the rules by which marine bacterial communities assemble in these nutrient-enhanced phycospheres, specifically addressing the role of host resources in driving community coalescence. Synthetic systems with varying combinations of known exometabolites of marine phytoplankton were inoculated with seawater bacterial assemblages, and communities were transferred daily to mimic the average duration of natural phycospheres. We found that bacterial community assembly was predictable from linear combinations of the taxa maintained on each individual metabolite in the mixture, weighted for the growth each supported. Deviations from this simple additive resource model were observed, but also attributed to resource-based factors via enhanced bacterial growth when host metabolites were available concurrently. The ability of photosynthetic hosts to shape bacterial associates through excreted metabolites represents a mechanism by which microbiomes with beneficial effects on host growth could be recruited. In the surface ocean, resource-based assembly of host-associated communities may underpin the evolution and maintenance of microbial interactions and determine the fate of a substantial portion of Earth’s primary production. 

Fu et al., 2020, Microbiology Resource Announcements

Genome sequences and metagenome-assembled genome sequences of microbial communities enriched on phytoplankton exometabolites

Fu, He, C. B. Smith, S. Sharma, and M. A. Moran

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We report 11 bacterial draft genome sequences and 38 metagenome-assembled genomes (MAGs) from marine phytoplankton exometabolite enrichments. The genomes and MAGs represent marine bacteria adapted to the metabolite environment of phycospheres, organic matter-rich regions surrounding phytoplankton cells, and are useful for exploring functional and taxonomic attributes of phytoplankton-associated bacterial communities.

Kiene et al., 2019, Geophysical Research Letters

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

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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.

Moran and Durham, 2019, Nature Reviews Microbiology

Sulfur Metabolites in the Pelagic Ocean

Mary Ann Moran and Bryndan P. Durham

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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. 

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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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.

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 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.