<i>Arcobacter peruensis</i> sp. nov., a Chemolithoheterotroph Isolated from Sulfide- and Organic-Rich Coastal Waters off Peru

Abstract

Members of the epsilonproteobacterial genus <i>Arcobacter</i> have been identified to be potentially important sulfide oxidizers in marine coastal, seep, and stratified basin environments. In the highly productive upwelling waters off the coast of Peru, <i>Arcobacter</i> cells comprised 3 to 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 <i>Arcobacter</i> population exceeded 10⁶ cells ml^-1 and where high rates of denitrification (up to 6.5 ± 0.4 μM N day^-1) and dark carbon fixation (2.8 ± 0.2 μM C day^-1) were measured, we isolated a previously uncultivated <i>Arcobacter</i> species, <i>Arcobacter peruensis</i> sp. nov. (BCCM LMG-31510). Genomic analysis showed that <i>A. peruensis</i> possesses genes encoding 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 <i>A. peruensis</i> genome. Physiological experiments demonstrated that <i>A. peruensis</i> grew best on a mix of sulfide, nitrate, and acetate. Isotope labeling experiments further verified that <i>A. peruensis</i> completely reduced nitrate to N₂ and assimilated acetate but did not fix CO₂, thus coupling heterotrophic growth to sulfide oxidation and denitrification. Single-cell nanoscale secondary ion mass spectrometry analysis of samples taken from shipboard isotope labeling experiments also confirmed that the <i>Arcobacter</i> population <i>in situ</i> did not substantially fix CO₂ The efficient growth yield associated with the chemolithoheterotrophic metabolism of <i>A. peruensis</i> may allow this <i>Arcobacter</i> species to rapidly bloom in eutrophic and sulfide-rich waters off the coast of Peru.<b>IMPORTANCE</b> Our multidisciplinary approach provides new insights into the ecophysiology of a newly isolated environmental <i>Arcobacter</i> species, as well as the physiological flexibility within the <i>Arcobacter</i> genus and sulfide-oxidizing, denitrifying microbial communities within oceanic oxygen minimum zones (OMZs). The chemolithoheterotrophic species <i>Arcobacter peruensis</i> 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, L. A. Levin, A. Oschlies, M. Grégoire, et al., Science 359:eaam7240, 2018, https://doi.org/10.1126/science.aam7240), niches where sulfide-oxidizing, denitrifying heterotrophs such as <i>A. peruensis</i> thrive are likely to expand.