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Abstract

Members of the epsilonproteobacterial genus Arcobacter 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, Arcobacter cells
comprised 3 to 25% of the total microbial community at a near-shore
station where sulfide concentrations exceeded 20 mu M in bottom waters.
From the chemocline where the Arcobacter population exceeded 10(6) cells
ml(-1) and where high rates of denitrification (up to 6.5 +/- 0.4 mu M N
day(-1)) and dark carbon fixation (2.8 +/- 0.2 mu M C day(-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 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 N-2 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 Arcobacter 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 species
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, L. A. Levin, A.
Oschlies, M. Gregoire, et al., Science 359:eaam7240, 2018,
https://doi.org/10.1126/science.aam7240), niches where
sulfide-oxidizing, denitrifying heterotrophs such as A. peruensis thrive
are likely to expand.