Abstract
Marine Benthic Group D (MBG-D) archaea, discovered by 16S rRNA gene survey decades ago, are ecologically important, yet understudied and uncultured sedimentary archaea. In this study, a comprehensive meta-analysis based on the 16S rRNA genes of MBG-D archaea showed that MBG-D archaea are one of the most frequently found archaeal lineages in global sediment with widespread distribution and high abundance, including 16 subgroups in total. Interestingly, some subgroups show significant segregations toward salinity and methane seeps. Co-occurrence analyses indicate significant non-random association of MBG-D archaea with Lokiarchaeota (in both saline and freshwater sediments) and Hadesarchaea, suggesting potential interactions among these archaeal groups. Meanwhile, based on four nearly complete metagenome-assembled genomes (MAGs) and corresponding metatranscriptomes reconstructed from mangrove and intertidal mudflat sediments, we provide insights on metabolic potentials and ecological functions of MBG-D archaea. MBG-D archaea appear to be capable of transporting and assimilating peptides and generating acetate and ethanol through fermentation. Metatranscriptomic analysis suggests high expression of genes for acetate and amino acid utilization and for peptidases, especially the M09B-type extracellular peptidase (collagenase) showing high expression levels in all four mangrove MAGs. Beyond heterotrophic central carbon metabolism, the MBG-D genomes include genes that might encode two autotrophic pathways: Wood–Ljundahl (WL) pathways using both H4MPT and H4folate as C1 carriers, and an incomplete dicarboxylate/4-hydroxybutyrate cycle with alternative bypasses from pyruvate to malate/oxaloacetate during dicarboxylation. These findings reveal MBG-D archaea as an important ubiquitous benthic sedimentary archaeal group with specific mixotrophic metabolisms, so we proposed the name Thermoprofundales as a new Order within the Class Thermoplasmata. Globally, Thermoprofundales and other benthic archaea might synergistically transform benthic organic matter, possibly playing a vital role in sedimentary carbon cycle.
Highlights
Archaea in the subsurface ecosystem play crucial roles in global biogeochemical cycles
Marine Benthic Group D (MBG-D) archaea have long been recognized from 16S rRNA gene surveys in benthic environments, and their global distribution and abundance place them as universal players in both terrestrial and marine subsurface realms (Supplementary Table S1) [5, 7,8,9]
The samples for metatranscriptomic analysis were sampled from the same sites and layers as those used for metagenomes at a later time
Summary
Archaea in the subsurface ecosystem play crucial roles in global biogeochemical cycles. Cell membrane lipid studies show evidence of more living archaea than bacteria [2] and archaea possessing the active metabolic capacity to assimilate sedimentary organic compounds [3] Within these subsurface environmental settings, the general archaeal cosmopolitans, such as Marine Benthic Group B (MBG-B), Marine Benthic Group D (MBG-D), and Bathyarchaeota, are dominant archaeal groups, which might contribute significantly to biogeochemical cycles [3,4,5,6]. A metagenomic survey reveals that MBG-D archaea and Bathyarchaeota co-exist in White Oak River estuary sediments with high abundance, sharing similar inferred metabolic capacities for acetogenesis and protein degradation in estuarine organic-rich regimes [14, 15] Owing to their potential importance in carbon transformation and ubiquitous distribution, it is important to have a broader view of the ecological, genomic, and metabolic understanding of MBG-D archaea. We addressed the relationships of distribution patterns to metabolic capacities and proposed the potential biogeochemical roles of these ubiquitous sedimentary archaea in carbon cycling
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Free) 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
