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.
Highlights
Subseafloor sediments harbor more than half of the oceans’ microorganisms (Kallmeyer et al, 2012; Parkes et al, 2014)
Calculating the total genome size of the seven Desulfatiglans-related single-cell genomes (SAGs) from the CheckM genome completeness estimates (Table 1) give values between 4.3 and 6.2 Mbp, which is within the range of the genome sizes of D. anilini and NaphS2
Large variation in genome size exists among known deltaproteobacterial sulfate reducers and for example the sulfate reducers Desulfonauticus submarinus DSM15269 and Desulfomicrobium thermophilum DSM16697 have genome sizes of 2.1 and 2.4 Mbp, respectively (IMG, genome IDs 2619619038 and 2571042920)
Summary
Subseafloor sediments harbor more than half of the oceans’ microorganisms (Kallmeyer et al, 2012; Parkes et al, 2014). Subseafloor microbial communities are buried in the sediment over time due to sedimentation. During burial they experience a successive change in geochemical conditions and increasing organic carbon limitation with sediment depth (Middelburg, 1989; Canfield and Thamdrup, 2009; Langerhuus et al, 2012; Lomstein et al, 2012). Starnawski et al (2017) concluded that such adaptations are present in a population before being buried in subsurface sediments, as the number of generations that microorganisms undergo during burial into deeper sediment layers likely does not allow for in situ adaptive evolution. Adaptations that allow microorganisms to survive under increasing energy limitation are, poorly understood and remain a challenge to investigate
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