Arcobacter peruensis sp.nov., a chemolithoheterotroph isolated from sulfide and organic rich coastal waters off Peru

Members of the epsilonproteobacterial genus Arcobacter have been identified as potentially important sulfide oxidizers in marine coastal, seep and stratified basin environments. In the highly productive upwelling waters off the coast of Peru, Arcobacter cells comprised 3-25% of the total microbial community at a near-shore station where sulfide concentrations exceeded 20 μM in bottom waters. From the chemocline where the Arcobacter population exceeded 106 cells ml-1, and where high rates of denitrification (up to 6.5 ± 0.4 μM N d-1) and dark carbon fixation (2.8 ± 0.2 μM C d-1) were measured, we isolated a previously uncultivated Arcobacter species - Arcobacter peruensis sp. nov. (BCCM LMG-31510) Genomic analysis showed that A. peruensis possesses genes encoding for sulfide oxidation and denitrification pathways, but lacks the ability to fix CO2 via autotrophic carbon fixation pathways. Genes encoding transporters for organic carbon compounds, however, were present in the A. peruensis genome. Physiological experiments demonstrated that A. peruensis grew best on a mix of sulfide, nitrate and acetate. Isotope labeling experiments further verified that A. peruensis completely reduced nitrate to N2 and assimilate acetate, but did not fix CO2, thus coupling heterotrophic growth to sulfide oxidation and denitrification. Single-cell nanoSIMS analysis of samples taken from shipboard isotope labeling experiments also confirmed that the Arcobacter spp. population in situ did not substantially fix CO2. The efficient growth yield associated with the chemolithoheterotrophic metabolism of A. peruensis may allow this Arcobacter species to rapidly bloom in eutrophic and sulfide-rich waters off the coast of Peru. Importance Our multidisciplinary approach provides new insights into the ecophysiology of a newly-isolated environmental Arcobacter species, as well as the physiological flexibility within the Arcobacter genus and sulfide-oxidizing, denitrifying microbial communities within oceanic oxygen minimum zones (OMZs). The chemolithoheterotrophic Arcobacter peruensis may play a substantial role in the diverse consortium of bacteria that is capable of coupling denitrification and fixed nitrogen loss to sulfide oxidation in eutrophic, sulfidic coastal waters. With increasing anthropogenic pressures on coastal regions, e.g. eutrophication and deoxygenation (D. Breitburg, et al., Science 359:eaam7240, 2018 DOI: 10.1126/science.aam7240), niches where sulfide-oxidizing, denitrifying heterotrophs such as A. peruensis thrive are likely to expand.