Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments

Abstract

Members of the archaeal phylum Bathyarchaeota are widespread and abundant in the energy-deficient marine subsurface sediments. However, their life strategies have remained largely elusive. Here, we provide genetic evidence that some lineages of Bathyarchaeota are acetogens, being capable of homoacetogenesis, a metabolism so far restricted to the domain Bacteria. Metabolic reconstruction based on genomic bins assembled from the metagenome of deep-sea subsurface sediments shows that the metabolism of some lineages of Bathyarchaeota is similar to that of bona fide bacterial homoacetogens, by having pathways for acetogenesis and for the fermentative utilization of a variety of organic substrates. Heterologous expression and activity assay of the acetate kinase gene ack from Bathyarchaeota, demonstrate further the capability of these Bathyarchaeota to grow as acetogens. The presence and expression of bathyarchaeotal genes indicative of active acetogenesis was also confirmed in Peru Margin subsurface sediments where Bathyarchaeota are abundant. The analyses reveal that this ubiquitous and abundant subsurface archaeal group has adopted a versatile life strategy to make a living under energy-limiting conditions. These findings further expand the metabolic potential of Archaea and argue for a revision of the role of Archaea in the carbon cycle of marine sediments.

Distribution of Bathyarchaeota Communities Across Different Terrestrial Settings and Their Potential Ecological Functions

“…It should be noted that in our research TOC also significantly shaped the distribution of MCG on a large scale. Even through the knowledge about MCG life style is still limited, several lines of evidence support the heterotrophic lifestyle of MCG recently131518. Our observation of the significant impact of TOC on MCG distribution may mount another line of heterotrophic lifestyle of MCG28.…”

“…Meanwhile, acetate is also a necessary growth factor for hydrogenotrophic Methanoregula 32, Methanocella 33 and Methanomicrobiaceae34. Importantly, some MCG members were demonstrated to possess a gene encoding acetate kinase18, which is involved in acetate production. This may explain the mechanism of symbiosis between MCG and Methanomicrobia.…”

“…Another line of evidence of its heterotrophic lifestyle is that detection of the gene encoding extracellular protein-degrading enzyme by single-cell sequencing15. Besides, some assembled genomes of MCG showed that they may capable of hydrolyzing extracellular plant-derived carbohydrates16, utilizing various methylated compounds for methylotrophic methanogenesis17 and fermenting organic substrates for acetogenesis18. Furthermore, the expression of the gene involved in degradation of aromatic compounds in MCG has been demonstrated with protocatechuate as the substrate19.…”

Metatranscriptomic Analysis Reveals Unexpectedly Diverse Microbial Metabolism in a Biogeochemical Hot Spot in an Alluvial Aquifer

“…Bathyarchaeota, particularly bin 89, had a disproportionately large presence in the metatranscriptomes of all samples, although this phylum is best known for its occurrence in marine, estuarine, and freshwater sediments (Meng et al, 2014; Evans et al, 2015; He et al, 2016; Lazar et al, 2016). Below, we elaborate on these findings in the context of how they build and expand on knowledge from existing studies of Rifle NRZs.…”

The role of archaea in the origin of eukaryotes

“…В геноме Lokiarchaeum обнаружен полный набор генов, кодирующих ацетил-KoA-путь, обеспечивающий воз-можность метаногенеза (которого нет у Lokiarchaeum) и автотрофной СО 2 -фиксации. Высказано предположе-ние [58] о том, что у Lokiarchaeum, как и у протеоархеи Bathyarchaeum (выявленной в метагеноме экосистемы морского бентоса) [60], может функционировать аце-тогенный путь, связанный со сбраживанием пептидов/ аминокислот и сопряженный с комбинированным мета-болическим процессом [61]. Можно полагать, что в бли-жайшее время трудности в изучении клеток новых линий архей будут преодолены и процессы энергетического метаболизма Loki-подобных архей будут расшифрованы, что позволит понять биохимическую природу синтро-физма, обеспечившего формирование LECA.…”