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Samo, T. J.

Publications and source records attributed to Samo, T. J..

4 recordsLinked to original sources

An algicidal bacterium shapes the microbiome during outdoor diatom cultivation collapse

Biogeochemistry and productivity of algae-dominated environments is fundamentally influenced by the diversity and activity of bacteria. Namely, algicidal bacteria that prey on algal hosts can control elemental cycling and host populations within outdoor algal ponds used for biofuel production. In this study, we describe the genomic and proteomic signatures of a putative algicidal bacterium, Kordia sp. (family Flavobacteriaceae), that bloomed during a population-wide crash of the biofuel diatom, Phaeodactylum tricornutum. This Kordia sp. bloom occurred after 29 days of cultivation in outdoor algal raceway ponds inoculated with P. tricornutum, but not in parallel ponds inoculated with Microchloropsis salina. Several signatures of antagonism expressed by Kordia during diatom demise highlights previously unexplored mechanisms that may aid in algicidal activity or bacterial competition, including the type VI secretion system and hydrogen peroxide production. Analysis of accompanying downstream microbiota (primarily of the Rhodobacteraceae family) provides evidence that cross-feeding is important in supporting microbial diversity during algal demise. Specifically, in situ and laboratory data suggest that Kordia acts as a primary degrader of biopolymers during algal demise, and co-occurring Rhodobacteraceae exploit degradation molecules or scavenge metabolic byproducts for carbon. Further, targeted analysis of 30 Rhodobacteraceae metagenome assembled genomes suggest algal pond Rhodobacteraceae commonly harbor pathways for carbon monoxide oxidation, a potential strategy to persist under competition. Collectively, these observations further constrain the role of algicidal bacteria in the aquatic ecosystem.

microbiology↗

THE DUAL ROLE OF THE MICROCYSTIS AERUGINOSA MICROBIOME ON CYANOTOXIN PRODUCTION: COMPETITION FOR AND REMINERALIZATION OF ORGANIC NITROGEN

Nutrient-induced blooms of the globally abundant freshwater toxic cyanobacterium Microcystis are the cause of worldwide public and ecosystem health concerns. The response of Microcystis growth and toxin production to new and recycled nitrogen (N) inputs, and the impact of heterotrophic bacteria in the Microcystis phycosphere on these processes are not well understood. Here, using microbiome transplant experiments, cyanotoxin analysis, and stable isotope tracing to measure N incorporation and exchange at single cell resolution, we monitored the growth, cyanotoxin production, and microbiome community structure of several Microcystis strains grown on amino acids and proteins as the sole N source. We demonstrate that 1) organic N availability shapes the microbiome community structure in the Microcystis phycosphere; 2) external organic N input leads to lower bacterial colonization of the phycosphere; 3) certain Microcystis strains can directly uptake amino acids, but with lower rates than heterotrophic bacteria; 4) biomass-specific microcystin production is not impacted by N source (i.e., nitrate, amino acids and protein) but rather by total N availability; and 5) some bacterial communities compete with Microcystis for organic N, but others remineralize organic N, in the process producing bio-available N for Microcystis. We conclude that organic N input can support Microcystis blooms and toxin production, and Microcystis-associated microbial communities play critical roles by influencing cyanobacterial succession through either decreasing (via competition) or increasing (via remineralization) N availability, especially under inorganic N scarcity.

microbiology↗

Single cell carbon and nitrogen incorporation and remineralization profiles are uncoupled from phylogenetic groupings of diatom-associated bacteria

Bacterial remineralization of algal organic matter is thought to fuel algal growth, but this has not been quantified. Consequently, we cannot currently predict whether some bacterial taxa may provide more remineralized nutrients to algae than others, nor whether this is linked their incorporation. We quantified bacterial incorporation of algal-derived complex dissolved organic C (DOC) and N (DON) and net algal incorporation of remineralized C and N at the single cell level using isotope tracing and NanoSIMS for fifteen bacterial co-cultures growing with the diatom Phaeodactylum tricornutum. We found unexpected variability in the net C and N fluxes between algae and bacteria, including non-ubiquitous complex DON utilization and remineralization. We identified three distinct functional categories of metabolic interactions, which we termed macromolecule remineralizers, macromolecule users, and small-molecule users, the latter exhibiting efficient growth under low carbon availability. The functional categories were not linked to phylogeny and could not be elucidated strictly from metabolic capacity as predicted by comparative genomics. Using comparative proteogenomic analyses, we show that a complex DON incorporating strain expressed proteins related to growth and peptide transport, and a non-incorporator prioritized reactive oxygen species scavenging and inorganic nutrient uptake. Our analysis suggests that phylogeny does not predict the extent of algae-bacteria metabolite exchange, and activity-based measurements are indispensable to classify the high diversity of microbes into functional groups. These categorizations are useful for conceptual understanding and mechanistic numerical modeling to ultimately predict the fate of elemental cycles in response to environmental change.

microbiology↗

A proton pump enhancing photosynthesis links phagocytosis to marine phytoplankton symbiogenesis

Diatoms, dinoflagellates, and coccolithophorids are the dominant groups of marine eukaryotic phytoplankton collectively responsible for the majority of primary production in the ocean1. These phytoplankton contain additional intracellular membranes around their chloroplasts derived from ancestral engulfment of red microalgae by unicellular heterotrophic eukaryotes that led to secondary endosymbiosis2. This symbiogenesis hypothesis for the origin of modern secondary endosymbiotic phytoplankton is supported by a wealth of palaeontologic, morphologic, and genomic evidence3-6. However, the selectable evolutionary advantage of these membranes and the physiological significance for extant phytoplankton are unknown. We report that the proton-pumping enzyme V-type H+-ATPase (VHA), ubiquitously used in eukaryotic intercellular digestion, is localized around the chloroplasts of centric diatoms and that VHA-activity significantly enhances photosynthesis over a wide range of oceanic irradiances. Similar results in pennate diatoms, dinoflagellates, and coccolithophorids, but not green or red microalgae, imply a mechanism resulting from the co-option of phagocytic VHA activity into a carbon concentrating mechanism that is common to secondary endosymbiotic phytoplankton. Furthermore, analogous VHA-dependent mechanisms in extant photosymbiotic marine invertebrates7-9 provide functional evidence for an adaptive advantage throughout the transition from endosymbiosis to symbiogenesis. Our results suggest that VHA-dependent enhancement of photosynthesis contributes at least 7% of primary production in the ocean, providing an example of a symbiosis-derived evolutionary innovation with global environmental implications.

evolutionary biology↗