Abstract
Spirochaetes are frequently detected in anoxic hydrocarbon- and organohalide-polluted groundwater, but their role in such ecosystems has remained unclear. To address this, we studied a sulfate-reducing, naphthalene-degrading enrichment culture, mainly comprising the sulfate reducer Desulfobacterium N47 and the rod-shaped Spirochete Rectinema cohabitans HM. Genome sequencing and proteome analysis suggested that the Spirochete is an obligate fermenter that catabolizes proteins and carbohydrates, resulting in acetate, ethanol, and molecular hydrogen (H2) production. Physiological experiments inferred that hydrogen is an important link between the two bacteria in the enrichment culture, with H2 derived from fermentation by R. cohabitans used as reductant for sulfate reduction by Desulfobacterium N47. Differential proteomics and physiological experiments showed that R. cohabitans utilizes biomass (proteins and carbohydrates) released from dead cells of Desulfobacterium N47. Further comparative and community genome analyses indicated that other Rectinema phylotypes are widespread in contaminated environments and may perform a hydrogenogenic fermentative lifestyle similar to R. cohabitans. Together, these findings indicate that environmental Spirochaetes scavenge detrital biomass and in turn drive necromass recycling at anoxic hydrocarbon-contaminated sites and potentially other habitats.
Highlights
The bacterial phylum Spirochaetes is well known for its commensal and pathogenic species, among them the causative agents of syphilis and Lyme disease [1]
Through reconstructing the genomes of two other putative Rectinema species, we provide evidence that environmental Spirochaetes may generally contribute to necromass recycling in anoxic hydrocarbon- and organohalide-contaminated environments as well as other anoxic habitats
We identified putative hydrogenase genes in the genomes of both R. cohabitans and Desulfobacterium N47
Summary
The bacterial phylum Spirochaetes is well known for its commensal and pathogenic species, among them the causative agents of syphilis and Lyme disease [1]. Environmental Spirochaetes are present in many enrichment cultures that degrade hydrocarbons or chlorinated compounds under anoxic conditions, including toluene [4], naphthalene [5], alkanes [2], terephthalate [6], and trichloroethene [7, 8]. The relative abundances of Spirochaetes range from 1.4 to 20.8% in 10 reported sulfate-reducing or methanogenic hydrocarbondegrading enrichment cultures originating from hydrocarbon-contaminated groundwater, aquifer sediments, and oil sands tailings ponds [2, 9]. In these cultures, sulfatereducing or fermenting bacteria primarily mediate the anaerobic transformation of hydrocarbon compounds [10]. The functional role of the Spirochaetes has remained unresolved
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