AbstractMarine sediments comprise one of the largest environments on the planet, and their microbial inhabitants are significant players in global carbon and nutrient cycles. Recent studies using metagenomic techniques have shown the complexity of these communities and identified novel microorganisms from the ocean floor. Here, we obtained 77 metagenome-assembled genomes (MAGs) from the bacterial phylum Armatimonadota in the Guaymas Basin, Gulf of California, and the Bohai Sea, China. These MAGs comprise two previously undescribed classes within Armatimonadota, which we propose naming Hebobacteria and Zipacnadia. They are globally distributed in hypoxic and anoxic environments and are dominant members of deep-sea sediments (up to 1.95% of metagenomic raw reads). The classes described here also have unique metabolic capabilities, possessing pathways to reduce carbon dioxide to acetate via the Wood-Ljungdahl pathway (WLP) and generating energy through the oxidative branch of glycolysis using carbon dioxide as an electron sink, maintaining the redox balance using the WLP. Hebobacteria may also be autotrophic, not previously identified in Armatimonadota. Furthermore, these Armatimonadota may play a role in sulfur and nitrogen cycling, using the intermediate compounds hydroxylamine and sulfite. Description of these MAGs enhances our understanding of diversity and metabolic potential within anoxic habitats worldwide.
AbstractMicrobes in marine sediments play crucial roles in global carbon and nutrient cycling. However, our understanding of microbial diversity and physiology on the ocean floor is limited. Here, we use phylogenomic analyses of thousands of metagenome-assembled genomes (MAGs) from coastal and deep-sea sediments to identify 55 MAGs that are phylogenetically distinct from previously described bacterial phyla. We propose that these MAGs belong to 4 novel bacterial phyla (Blakebacterota, Orphanbacterota, Arandabacterota, and Joyebacterota) and a previously proposed phylum (AABM5-125-24), all of them within the FCB superphylum. Comparison of their rRNA genes with public databases reveals that these phyla are globally distributed in different habitats, including marine, freshwater, and terrestrial environments. Genomic analyses suggest these organisms are capable of mediating key steps in sedimentary biogeochemistry, including anaerobic degradation of polysaccharides and proteins, and respiration of sulfur and nitrogen. Interestingly, these genomes code for an unusually high proportion (~9% on average, up to 20% per genome) of protein families lacking representatives in public databases. Genes encoding hundreds of these protein families colocalize with genes predicted to be involved in sulfur reduction, nitrogen cycling, energy conservation, and degradation of organic compounds. Our findings advance our understanding of bacterial diversity, the ecological roles of these bacteria, and potential links between novel gene families and metabolic processes in the oceans.
AbstractThe subsurface biosphere is largely unexplored and contains a broad diversity of uncultured microbes1. Despite being one of the few prokaryotic lineages that is cosmopolitan in both the terrestrial and marine subsurface2–4, the physiological and ecological roles of SAGMEG (South-African Gold Mine Miscellaneous Euryarchaeal Group) Archaea are unknown. Here, we report the metabolic capabilities of this enigmatic group as inferred from genomic reconstructions. Four high-quality (63–90% complete) genomes were obtained from White Oak River estuary and Yellowstone National Park hot spring sediment metagenomes. Phylogenomic analyses place SAGMEG Archaea as a deeply rooting sister clade of the Thermococci, leading us to propose the name Hadesarchaea for this new Archaeal class. With an estimated genome size of around 1.5 Mbp, the genomes of Hadesarchaea are distinctly streamlined, yet metabolically versatile. They share several physiological mechanisms with strict anaerobic Euryarchaeota. Several metabolic characteristics make them successful in the subsurface, including genes involved in CO and H2 oxidation (or H2 production), with potential coupling to nitrite reduction to ammonia (DNRA). This first glimpse into the metabolic capabilities of these cosmopolitan Archaea suggests they are mediating key geochemical processes and are specialized for survival in the subsurface biosphere.
Metagenomics has provided access to genomes of as yet uncultivated microorganisms in natural environments, yet there are gaps in our knowledge—particularly for Archaea—that occur at relatively low abundance and in extreme environments. Ultrasmall cells (<500 nm in diameter) from lineages without cultivated representatives that branch near the crenarchaeal/euryarchaeal divide have been detected in a variety of acidic ecosystems. We reconstructed composite, near-complete ~1-Mb genomes for three lineages, referred to as ARMAN (archaeal Richmond Mine acidophilic nanoorganisms), from environmental samples and a biofilm filtrate. Genes of two lineages are among the smallest yet described, enabling a 10% higher coding density than found genomes of the same size, and there are noncontiguous genes. No biological function could be inferred for up to 45% of genes and no more than 63% of the predicted proteins could be assigned to a revised set of archaeal clusters of orthologous groups. Some core metabolic genes are more common in
Crenarchaeota
than
Euryarchaeota
, up to 21% of genes have the highest sequence identity to bacterial genes, and 12 belong to clusters of orthologous groups that were previously exclusive to bacteria. A small subset of 3D cryo-electron tomographic reconstructions clearly show penetration of the ARMAN cell wall and cytoplasmic membranes by protuberances extended from cells of the archaeal order
Thermoplasmatales
. Interspecies interactions, the presence of a unique internal tubular organelle [Comolli, et al. (2009)
ISME J
3:159–167], and many genes previously only affiliated with Crenarchaea or Bacteria indicate extensive unique physiology in organisms that branched close to the time that
Cren
- and
Euryarchaeotal
lineages diverged.
ABSTRACT
During a molecular phylogenetic survey of extremely acidic (pH < 1), metal-rich acid mine drainage habitats in the Richmond Mine at Iron Mountain, Calif., we detected 16S rRNA gene sequences of a novel bacterial group belonging to the order
Rickettsiales
in the
Alphaproteobacteria
. The closest known relatives of this group (92% 16S rRNA gene sequence identity) are endosymbionts of the protist
Acanthamoeba
. Oligonucleotide 16S rRNA probes were designed and used to observe members of this group within acidophilic protists. To improve visualization of eukaryotic populations in the acid mine drainage samples, broad-specificity probes for eukaryotes were redesigned and combined to highlight this component of the acid mine drainage community. Approximately 4% of protists in the acid mine drainage samples contained endosymbionts. Measurements of internal pH of the protists showed that their cytosol is close to neutral, indicating that the endosymbionts may be neutrophilic. The endosymbionts had a conserved 273-nucleotide intervening sequence (IVS) in variable region V1 of their 16S rRNA genes. The IVS does not match any sequence in current databases, but the predicted secondary structure forms well-defined stem loops. IVSs are uncommon in rRNA genes and appear to be confined to bacteria living in close association with eukaryotes. Based on the phylogenetic novelty of the endosymbiont sequences and initial culture-independent characterization, we propose the name “
Candidatus
Captivus acidiprotistae.” To our knowledge, this is the first report of an endosymbiotic relationship in an extremely acidic habitat.