Abstract
Marine sediments are frequently covered by mats of the filamentous Beggiatoa and other large nitrate-storing bacteria that oxidize hydrogen sulfide using either oxygen or nitrate, which they store in intracellular vacuoles. Despite their conspicuous metabolic properties and their biogeochemical importance, little is known about their genetic repertoire because of the lack of pure cultures. Here, we present a unique approach to access the genome of single filaments of Beggiatoa by combining whole genome amplification, pyrosequencing, and optical genome mapping. Sequence assemblies were incomplete and yielded average contig sizes of approximately 1 kb. Pathways for sulfur oxidation, nitrate and oxygen respiration, and CO2 fixation confirm the chemolithoautotrophic physiology of Beggiatoa. In addition, Beggiatoa potentially utilize inorganic sulfur compounds and dimethyl sulfoxide as electron acceptors. We propose a mechanism of vacuolar nitrate accumulation that is linked to proton translocation by vacuolar-type ATPases. Comparative genomics indicates substantial horizontal gene transfer of storage, metabolic, and gliding capabilities between Beggiatoa and cyanobacteria. These capabilities enable Beggiatoa to overcome non-overlapping availabilities of electron donors and acceptors while gliding between oxic and sulfidic zones. The first look into the genome of these filamentous sulfur-oxidizing bacteria substantially deepens the understanding of their evolution and their contribution to sulfur and nitrogen cycling in marine sediments.
Highlights
Mats of conspicuously large sulfur-oxidizing bacteria often cover the seafloor in organicly rich coastal areas, at hydrate ridge methane seeps, at hydrothermal vents, on whale falls, and in coastal upwelling regions [1,2,3,4,5]
We identified 47 ribosomal proteins in the PS dataset that exclusively affiliated with Gammaproteobacteria (Table S4)
Because of the incomplete assembly, three non-overlapping fragments of a NarG gene were found (BgP3372, BgP5024, and sequences downstream of BgP4047) that were concatenated and phylogenetically affiliated with Proteobacteria (Figure S6). In addition to these proteobacterial NarGH, we surprisingly identified a second nitrate reductase, NarGH (BgP0139 and BgP4784), displaying by far the highest sequence similarities (NarG: 57% similarity at 98% coverage) to a putative nitrate reductase/nitrite oxidoreductase of the anaerobically ammonia-oxidizing planctomycete Kuenenia stuttgartiensis [56]
Summary
Mats of conspicuously large sulfur-oxidizing bacteria often cover the seafloor in organicly rich coastal areas, at hydrate ridge methane seeps, at hydrothermal vents, on whale falls, and in coastal upwelling regions [1,2,3,4,5]. The closely related genera Beggiatoa, Thioploca, and Thiomargarita are among the largest prokaryotes known, and they usually contain a vacuole that can account for up to 90% of the cell volume [6] On the seafloor these large sulfur-oxidizing bacteria fulfill an important ecological function by preventing the release of toxic hydrogen sulfide from the sediment into the water column. Oxygen has been regarded as the major electron acceptor coupled to sulfur oxidation; there is growing evidence that when experiencing anoxia these large vacuolated Beggiatoa, Thioploca, and Thiomargarita respire nitrate, which they concentrate up to 10,000-fold (;500 mM) within their intracellular vacuoles [5,12,13] Their nitrate and sulfur storage capacities allow them to bridge the suboxic zone, where neither sulfide nor oxygen is detectable, which gives them an advantage over other sulfideoxidizing bacteria.
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