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1. Bacterial transcriptional response to picoeukaryote Micromonas commoda

   https://doi.org/10.26008/1912/bco-dmo.928039.1  

   Moran, Mary Ann; Hamilton, Maria; Ferrer-González, Frank X; Smith, Christa; Ferrer-González, Frank X; Moran, Mary Ann; Smith, Christa (July 2024, Biological and Chemical Oceanography Data Management Office (BCO-DMO))

   Marine biogeochemical cycles are built on interactions between surface ocean microbes, particularly those connecting phytoplankton primary producers to heterotrophic bacteria. However, direct influences of bacteria on phytoplankton physiology are poorly known. In this study, three marine bacteria (Ruegeria pomeroyi DSS-3, Stenotrophomonas sp. SKA14, and Polaribacter dokdonensis MED152) were co-cultured with green alga Micromonas commoda, and the phytoplankter's transcriptome was studied by RNASeq. The presence of each bacterium invoked transcriptomic remodeling by M. commoda after 8 h in co-culture. Some aspects of the algal transcriptomic response were conserved across all three bacteria, while others were restricted to a single bacterium. M. commoda had both rapid and extensive responses to heterotrophic bacteria. 

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2. Rival phytoplankton contribute to the cross protection of Prochlorococcus from oxidative stress

   https://doi.org/10.1128/aem.01128-24  

   Calfee, Benjamin C; Bowden, Emily C; Zinser, Erik R (May 2025, Applied and Environmental Microbiology)

   Bose, Arpita (Ed.)

   ABSTRACT The marine cyanobacteriumProchlorococcusnumerically dominates the phytoplankton communities in all lower latitude, open ocean environments. Having lost the catalase gene,Prochlorococcusis highly susceptible to exogenous hydrogen peroxide (H₂O₂) produced at the ocean’s surface. Protection by H₂O₂-scavenging heterotrophic “helper” bacteria has been demonstrated in laboratory cultures and implicated as an important mechanism ofProchlorococcussurvival in the ocean. Importantly, some other phytoplankton can also scavenge H₂O₂, suggesting these competing microbes may inadvertently protectProchlorococcus. In this study, we assessed the ability of co-occurring phytoplankton, the cyanobacteriumSynechococcusand picoeukaryotesMicromonasandOstreococcus, to protectProchlorococcusfrom H₂O₂exposure when cocultured at ecologically relevant abundances. All three genera could significantly degrade H₂O₂and diminishProchlorococcusmortality during H₂O₂exposures simulating photochemical production and rainfall events. We suggest that these phytoplankton groups contribute significantly to the H₂O₂microbial sink of the open ocean, thus complicating their relationships with and perhaps contributing to the evolutionary history ofProchlorococcus.IMPORTANCEThe marine cyanobacteriumProchlorococcusis the most abundant photosynthetic organism on the planet and is crucially involved in microbial community dynamics and biogeochemical cycling in most tropical and subtropical ocean waters. This success is due, in part, to the detoxification of the reactive oxygen species hydrogen peroxide (H₂O₂) performed by “helper” organisms. Earlier work identified heterotrophic bacteria as helpers, and here, we demonstrate that rival cyanobacteria and picoeukaryotic phytoplankton can also contribute to the survival ofProchlorococcusduring exposure to H₂O₂. Whereas heterotrophic bacteria helper organisms can benefit directly from promoting the survival of carbon-fixingProchlorococcuscells, phytoplankton helpers may suffer a twofold injury: production of H₂O₂degrading enzymes constrains already limited resources in oligotrophic environments, and the activity of these enzymes bolsters the abundance of their numerically dominant competitor. These findings build toward a better understanding of the intricate dynamics and interactions that shape microbial community structure in the open ocean. 

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3. Dynamic reworking of marine diatom endometabolomes in response to temperature and a model bacterium

   https://doi.org/10.1128/msystems.01036-25  

   Olofsson, Malin; Uchimiya, Mario; Ferrer-González, Frank X; Schreier, Jeremy E; Powers, McKenzie A; Smith, Christa B; Edison, Arthur S; Moran, Mary Ann (January 2026, mSystems)

   Makhalanyane, Thulani P (Ed.)

   ABSTRACT A large annual carbon flux occurs through the surface ocean’s labile dissolved organic carbon (DOC) pool, with influx dominated by phytoplankton-derived metabolites and outflux by heterotrophic bacterioplankton uptake. We addressed the dynamics of this carbon flow between microbial primary and secondary producers through analysis of theThalassiosira pseudonanaCCMP1335 endometabolome, a proxy for the labile DOC released upon phytoplankton lysis, as temperature and bacterial presence were altered. Diatom strains acclimated at one of three different temperatures (14°C, 20°C, or 28°C) were cultured either axenically or with the bacteriumRuegeria pomeroyiDSS-3, and their endometabolites analyzed by NMR. Median concentration variation between conditions was ~1.5-fold across all identified endometabolites. Those with roles as osmolytes varied most, exhibiting concentration differences up to 170-fold across conditions with the largest variations triggered by the presence/absence of the heterotrophic bacterium. Differential expression observed for diatom metabolite synthesis pathways suggested changes in synthesis rates as a mechanism for endometabolome remodeling. Consistent with expectations of high turnover by heterotrophic bacteria, endometabolite mean lifetimes in a DOC pool were <2 h to 12 h. IMPORTANCEThe role of labile DOC in the transfer of marine carbon between phytoplankton and heterotrophic bacteria was first recognized 40 years ago, yet the identity and dynamics of phytoplankton metabolites entering the labile DOC pool are still poorly known. Using metabolome and transcriptome profiling, we found highly variable composition and concentration of diatom endometabolites, depending on growth conditions and arising over time frames as short as a single growth cycle. This strong response to external conditions, both biotic and abiotic, suggests that the chemical composition of phytoplankton intracellular pools released during lysis shift with ocean conditions. As phytoplankton cell lysis is one of the largest sources of labile dissolved compounds in the ocean, dynamic compositional changes in the metabolites released to heterotrophic bacteria have implications for the fate of surface ocean carbon. 

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4. Bacterial transcriptional response to labile exometabolites from photosynthetic picoeukaryote Micromonas commoda

   https://doi.org/10.1038/s43705-023-00212-0  

   Ferrer-González, Frank X.; Hamilton, Maria; Smith, Christa B.; Schreier, Jeremy E.; Olofsson, Malin; Moran, Mary Ann (December 2023, ISME Communications)

   Abstract Dissolved primary production released into seawater by marine phytoplankton is a major source of carbon fueling heterotrophic bacterial production in the ocean. The composition of the organic compounds released by healthy phytoplankton is poorly known and difficult to assess with existing chemical methods. Here, expression of transporter and catabolic genes by three model marine bacteria ( Ruegeria pomeroyi DSS-3, Stenotrophomonas sp. SKA14, and Polaribacter dokdonensis MED152) was used as a biological sensor of metabolites released from the picoeukaryote Micromonas commoda RCC299. Bacterial expression responses indicated that the three species together recognized 38 picoeukaryote metabolites. This was consistent with the Micromonas expression of genes for starch metabolism and synthesis of peptidoglycan-like intermediates. A comparison of the hypothesized Micromonas exometabolite pool with that of the diatom Thalassiosira pseudonana CCMP1335, analyzed previously with the same biological sensor method, indicated that both phytoplankton released organic acids, nucleosides, and amino acids, but differed in polysaccharide and organic nitrogen release. Future ocean conditions are expected to favor picoeukaryotic phytoplankton over larger-celled microphytoplankton. Results from this study suggest that such a shift could alter the substrate pool available to heterotrophic bacterioplankton. 

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5. Growth-stage-related shifts in diatom endometabolome composition set the stage for bacterial heterotrophy

   https://doi.org/10.1038/s43705-022-00116-5  

   Olofsson, Malin; Ferrer-González, Frank X.; Uchimiya, Mario; Schreier, Jeremy E.; Holderman, Nicole R.; Smith, Christa B.; Edison, Arthur S.; Moran, Mary Ann (December 2022, ISME Communications)

   Abstract Phytoplankton-derived metabolites fuel a large fraction of heterotrophic bacterial production in the global ocean, yet methodological challenges have limited our understanding of the organic molecules transferred between these microbial groups. In an experimental bloom study consisting of three heterotrophic marine bacteria growing together with the diatom Thalassiosira pseudonana , we concurrently measured diatom endometabolites (i.e., potential exometabolite supply) by nuclear magnetic resonance (NMR) spectroscopy and bacterial gene expression (i.e., potential exometabolite uptake) by metatranscriptomic sequencing. Twenty-two diatom endometabolites were annotated, with nine increasing in internal concentration in the late stage of the bloom, eight decreasing, and five showing no variation through the bloom progression. Some metabolite changes could be linked to shifts in diatom gene expression, as well as to shifts in bacterial community composition and their expression of substrate uptake and catabolism genes. Yet an overall low match indicated that endometabolome concentration was not a good predictor of exometabolite availability, and that complex physiological and ecological interactions underlie metabolite exchange. Six diatom endometabolites accumulated to higher concentrations in the bacterial co-cultures compared to axenic cultures, suggesting a bacterial influence on rates of synthesis or release of glutamate, arginine, leucine, 2,3-dihydroxypropane-1-sulfonate, glucose, and glycerol-3-phosphate. Better understanding of phytoplankton metabolite production, release, and transfer to assembled bacterial communities is key to untangling this nearly invisible yet pivotal step in ocean carbon cycling. 

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