Genome and physiology of a model Epsilonproteobacterium responsible for sulfide detoxification in marine oxygen depletion zones

Abstract

Eutrophication and global climate change lead to expansion of hypoxia in the ocean, often accompanied by the production of hydrogen sulfide, which is toxic to higher organisms. Chemoautotrophic bacteria are thought to buffer against increased sulfide concentrations by oxidizing hydrogen sulfide before its diffusion to oxygenated surface waters. Model organisms from such environments have not been readily available, which has contributed to a poor understanding of these microbes. We present here a detailed study of "Sulfurimonas gotlandica" str. GD1, an Epsilonproteobacterium isolated from the Baltic Sea oxic-anoxic interface, where it plays a key role in nitrogen and sulfur cycling. Whole-genome analysis and laboratory experiments revealed a high metabolic flexibility, suggesting a considerable capacity for adaptation to variable redox conditions. S. gotlandica str. GD1 was shown to grow chemolithoautotrophically by coupling denitrification with oxidation of reduced sulfur compounds and dark CO 2 fixation. Metabolic versatility was further suggested by the use of a range of different electron donors and acceptors and organic carbon sources. The number of genes involved in signal transduction and metabolic pathways exceeds those of other Epsilonproteobacteria. Oxygen tolerance and environmental-sensing systems combined with chemotactic responses enable this organism to thrive successfully in marine oxygen-depletion zones. We propose that S. gotlandica str. GD1 will serve as a model organism in investigations that will lead to a better understanding how members of the Epsilonproteobacteria are able to cope with water column anoxia and the role these microorganisms play in the detoxification of sulfidic waters. marine bacteria | sulfide oxidation | isolation | genomics

Productivity, metabolism and physiology of free-living chemoautotrophic Epsilonproteobacteria

“…Weerakoon and Olson (2008) also showed that this unusual mechanism is due to differences in the NuoE/F subunits that interact with NADH in canonical complex I. Interestingly, they note that S. denitrificans and other autotrophic Epsilonproteobacteria also possess non-canonical NuoEF subunits. So far, this different NuoEF composition has also been observed in all genomes of Sulfurimonas and Sulfurovum sequenced to date (Nakagawa et al, 2007;Sievert et al, 2008;Sikorski et al, 2010;Grote et al, 2012;Cai et al, 2014)…”

“…In contrast to the Nautiliales, nearly all Campylobacterales isolates reported thus far have the potential to use oxygen, and in some cases tolerate levels approaching atmospheric concentrations Takai et al, 2006). Even for those reported to be strict anaerobes, genome sequences contain a cbb 3 -type high-affinity cytochrome c oxidase (Grote et al, 2012;Cai et al, 2014), suggesting the ability to use oxygen as an electron acceptor is typical of autotrophic Campylobacterales. The use of nitrate and sulfur as electron acceptors is also common in this lineage but obligate aerobes do exist .…”

Activity and abundance of denitrifying bacteria in the subsurface biosphere of diffuse hydrothermal vents of the Juan de Fuca Ridge

“…NBC37-1; Inagaki et al, 2004) and Nitratifractor (i.e., Nitratifractor Salsuginis Nakagawa et al, 2005b). Additionally, Sievert et al (2008) and Grote et al (2012) reported that other ε-proteobacteria of the genus Sulfurimonas (Sulfurimonas denitrificans str. DMS1251 and Sulfurimonas gotlandica str.…”

“…Nitrogen is an essential macronutrient for all organisms, and oceanic N sinks that remove biologically available N via denitrification and anaerobic ammonium (NH N 2 gas, is mediated by both heterotrophic and autotrophic bacteria and occurs in the anoxic and suboxic oceanic water-column (Codispoti et al, 2001;Lavik et al, 2009;Ward et al, 2009;Grote et al, 2012) and sediments (e.g., Christensen et al, 1987). For the past decade, anammox, i.e., the conversion of NH + 4 and nitrite (NO − 2 ) to N 2 gas by autotrophic anaerobic bacteria, has also been reported to account for a significant part of the N loss in oceanic anoxic zones (Dalsgaard et al, 2003;Kuypers et al, 2003;2005;Lam et al, 2009;Jensen et al, 2011).…”

Motility in the epsilon-proteobacteria

“…Many are chemolithotrophs [11] that obtain energy by oxidizing compounds found in 32 their environment. The Sulfurospirillum, Sulfurimonas,Sulfuricurvum,Thiovulum,and some Arcobactergenera 33 from the Campylobacteralesorder are environmental bacteria [12,13], with habitats ranging from marine 34 hydrothermal vents and coastal sediments [14], underground oil-storage facilities [15], plant roots in salt 35 marsh sediments [16] and pond mud [17]. Intriguingly, there are multiple cases of epsilon-proteobacteria that 36 combine animal association with hydrothermal vent environments by establishing symbioses with gastropods 37 and annelids endemic to vents [18,19].…”