Single-Cell Genomics Reveals a Diverse Metabolic Potential of Uncultivated Desulfatiglans-Related Deltaproteobacteria Widely Distributed in Marine Sediment

Abstract

Desulfatiglans-related organisms comprise one of the most abundant deltaproteobacterial lineages in marine sediments where they occur throughout the sediment column in a gradient of increasing sulfate and organic carbon limitation with depth. Characterized Desulfatiglans isolates are dissimilatory sulfate reducers able to grow by degrading aromatic hydrocarbons. The ecophysiology of environmental Desulfatiglans-populations is poorly understood, however, possibly utilization of aromatic compounds may explain their predominance in marine subsurface sediments. We sequenced and analyzed seven Desulfatiglans-related single-cell genomes (SAGs) from Aarhus Bay sediments to characterize their metabolic potential with regard to aromatic compound degradation and energy metabolism. The average genome assembly size was 1.3 Mbp and completeness estimates ranged between 20 and 50%. Five of the SAGs (group 1) originated from the sulfate-rich surface part of the sediment while two (group 2) originated from sulfate-depleted subsurface sediment. Based on 16S rRNA gene amplicon sequencing group 2 SAGs represent the more frequent types of Desulfatiglans-populations in Aarhus Bay sediments. Genes indicative of aromatic compound degradation could be identified in both groups, but the two groups were metabolically distinct with regard to energy conservation. Group 1 SAGs carry a full set of genes for dissimilatory sulfate reduction, whereas the group 2 SAGs lacked any genetic evidence for sulfate reduction. The latter may be due to incompleteness of the SAGs, but as alternative energy metabolisms group 2 SAGs carry the genetic potential for growth by acetogenesis and fermentation. Group 1 SAGs encoded reductive dehalogenase genes, allowing them to access organohalides and possibly conserve energy by their reduction. Both groups possess sulfatases unlike their cultured relatives allowing them to utilize sulfate esters as source of organic carbon and sulfate. In conclusion, the uncultivated marine Desulfatiglans populations are metabolically diverse, likely reflecting different strategies for coping with energy and sulfate limitation in the subsurface seabed.

Organohalide-respiringDesulfolunaspecies isolated from marine environments

“…The OHR metabolism of strain DBB and of strain MSL71 ⊤ was verified in this study. In line with former reports [22–25], this study further reinforces an important role of marine organohalide-respiring Deltaproteobacteria in halogen, sulfur and carbon cycling.…”

“…Numerous studies have reported OHR activity and occurrence of OHRB and rdhA genes in marine environments [6, 19–21]. Recent genomic [22–24] and single-cell genomic [25] analyses revealed widespread occurrence of rdh gene clusters in marine Deltaproteobacteria , indicting untapped potential for OHR. Accordingly, OHR metabolism was experimentally verified in three Deltaproteobacteria strains, not previously known as OHRB [23].…”

Heterogeneity in Hyporheic Flow, Pore Water Chemistry, and Microbial Community Composition in an Alpine Streambed

“…Although the taxonomy is poorly defined, members of the Deltaproteobacteria are frequently detected in anoxic environments where they catalyze anaerobic metabolisms including metal and sulfate reduction. While we acknowledge the challenges in linking 16S rRNA marker gene data with functional potential, isolated Desulfatiglans species have previously been characterized as catalyzing enzymatic sulfate reduction (Jochum et al, ; Suzuki et al, ).…”

Organohalide-respiring Desulfoluna species isolated from marine environments

“…Numerous studies have reported OHR activity and occurrence of OHRB and rdhA genes in marine environments [6,[19][20][21]. Recent genomic [22][23][24] and single-cell genomic [25] analyses revealed widespread occurrence of rdh gene clusters in marine Deltaproteobacteria, indicting untapped potential for OHR. Accordingly, OHR metabolism was experimentally verified in three Deltaproteobacteria strains, not previously known as OHRB [23].…”