Publications

4499

Abstract Anoxic and hypoxic environments serve as habitats for diverse microorganisms, including unicellular eukaryotes (protists) and prokaryotes. To thrive in low-oxygen environments, protists and prokaryotes often establish specialized metabolic cross-feeding associations, such as syntrophy, with other microorganisms. Previous studies show that the breviate protist Lenisia limosa engages in a mutualistic association with a denitrifying Arcobacter bacterium based on hydrogen exchange. Here, we investigate if the ability to form metabolic interactions is conserved in other breviates by studying five diverse breviate microcosms and their associated bacteria. We show that five laboratory microcosms of marine breviates live with multiple hydrogen-consuming prokaryotes that are predicted to have different preferences for terminal electron acceptors using genome-resolved metagenomics. Protist growth rates vary in response to electron acceptors depending on the make-up of the prokaryotic community. We find that the metabolic capabilities of the bacteria and not their taxonomic affiliations determine protist growth and survival and present new potential protist-interacting bacteria from the Arcobacteraceae, Desulfovibrionaceae, and Terasakiella lineages. This investigation uncovers potential nitrogen and sulfur cycling pathways within these bacterial populations, hinting at their roles in syntrophic interactions with the protists via hydrogen exchange.

Abstract Phytoplankton are the base of marine food webs. They form intricate interactions with heterotrophic bacteria ranging from mutualistic to pathogenic that together impact oceanic carbon and nutrient cycling. Our understanding of these interactions in marine environments remains primarily limited to laboratory-based studies of model organisms. Here, we report the discovery and characterization of Ekhidna algicida sp. nov. strain To15, isolated from the oligotrophic Pacific Ocean (16°N, 140°W) based on its algicidal effect on the pelagic diatom Thalassiosira oceanica. Subsequent co-culture experiments demonstrate that E. algicida is lethal within days to a diverse array of diatoms, including diatoms isolated from similar locations, with the effect mediated by bacterial exudates produced during co-culture with susceptible diatoms. Exudates of E. algicida monoculture are not algicidal, suggesting a pathogenic shift upon interaction with susceptible diatoms. The genome of E. algicida To15 encodes for a type IX secretion system (T9SS), together with candidate secreted proteases, suggesting a potential protein-mediated pathogenicity. Twenty additional algicidal Ekhidna strains were subsequently isolated from the Pacific Ocean. All these algicidal bacteria pass through 0.2 μm pore-size filters, highlighting the importance of the often-overlooked group of “filterable” marine bacteria. Our findings reveal E. algicida as a Pacific Ocean diatom pathogen, with potential impacts on microbial community composition dynamics in pelagic ecosystems.