Publications

4511

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 Analysing the nitrogen (15ε) and oxygen (18ε) isotope effects of anaerobic ammonium oxidation (anammox) is essential for accurately assessing its potential contribution to fixed-N losses in the ocean, yet the 18ε of anammox remains unexplored. Here, we determined the previously unexplored 18ε of anammox using a highly enriched culture of the marine anammox species “Ca. Scalindua sp”. Because Scalindua significantly accelerated oxygen isotope exchange between NO2− and H2O, we introduced a new rate constant for anammox-mediated oxygen isotope exchange (keq, AMX = 8.44 ~ 13.56 × 10−2 h−1), which is substantially faster than abiotic oxygen isotope exchange (keq, abio = 1.13 × 10−2 h−1), into a numerical model to estimate the 18ε during anammox. Based on our experimental results, we successfully determined the 18ε associated with: (1) conversion of NO2− to N2 (18εNO2- → N2 = 10.6 ~ 16.1‰), (2) NO2− oxidation to NO3− (18εNO2- → NO3- = −2.9 ~ −11.0‰, inverse fractionation), (3) incorporation of oxygen from water during NO2− oxidation to NO3− (18εH2O = 16.4 ~ 19.2‰). Our study underscores the possibility that unique anammox oxygen isotope signals may be masked due to substantial anammox-mediated oxygen isotope exchange between NO2− and H2O. Therefore, careful consideration is required when utilizing δ18ONO3- and δ18ONO2- as geochemical markers to assess the potential contribution of anammox to fixed-N losses in the ocean.

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.