Groundwater Elusimicrobia are metabolically diverse compared to gut microbiome Elusimicrobia and some have a novel nitrogenase paralog

Abstract

Currently described members of Elusimicrobia, a relatively recently defined phylum, are animal-associated and rely on fermentation. However, free-living Elusimicrobia have been detected in sediments, soils and groundwater, raising questions regarding their metabolic capacities and evolutionary relationship to animal-associated species. Here, we analyzed 94 draftquality, non-redundant genomes, including 30 newly reconstructed genomes, from diverse animal-associated and natural environments. Genomes group into 12 clades, 10 of which previously lacked reference genomes. Groundwater-associated Elusimicrobia are predicted to be capable of heterotrophic or autotrophic lifestyles, reliant on oxygen or nitrate/nitrite-dependent respiration, or a variety of organic compounds and Rhodobacter nitrogen fixation (Rnf) complex-dependent acetogenesis with hydrogen and carbon dioxide as the substrates. Genomes from two clades of groundwater-associated Elusimicrobia often encode a new group of nitrogenase paralogs that co-occur with an extensive suite of radical S-Adenosylmethionine (SAM) proteins. We identified similar genomic loci in genomes of bacteria from the Gracilibacteria phylum and the Myxococcales order and predict that the gene clusters reduce a tetrapyrrole, possibly to form a novel cofactor. The animal-associated Elusimicrobia clades nest phylogenetically within two free-living-associated clades. Thus, we propose an evolutionary trajectory in which some Elusimicrobia adapted to animal-associated lifestyles from free-living species via genome reduction.

Patterns of Gene Content and Co-occurrence Constrain the Evolutionary Path toward Animal Association in Candidate Phyla Radiation Bacteria

“…Our results suggest that Saccharibacteria (and potentially Gracilibacteria) from the human/animal microbiome have smaller genome sizes than related, deeper-branching lineages of environmental origin. This pattern is also apparent for other, free-living groups adapted to the animal microbiome from the environment, like the Elusimicrobia ( 97 ) and intracellular symbionts of insects ( 98 ). However, in contrast to findings for Elusimicrobia, where host-associated lineages have common patterns of loss of metabolic capacities compared to relatives from nonhost environments ( 97 ), patterns of gene loss in animal-associated CPR bacteria appear to be heterogeneous and lineage specific.…”

Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale

“…Phylogenetic trees for proteins of interest were reconstructed using the same methods described above, except with different sets of reference sequences. East River homologs in the dimethyl sulfoxide reductase (DMSOR) superfamily such as the catalytic subunit of formate dehydrogenase (FdhA), nitrite oxidoreductase (NxrA), membrane-bound nitrate reductase (NarG; H + -translocating), and periplasmic nitrate reductase subunit A (NapA) were confirmed by phylogeny on a tree with reference sequences from Méheust et al [ 47 ] (Table S11, Additional file 16 and Data S5, Additional file 17 ). To distinguish form I and form II CODHs and other subtypes among homologs to K03520, we used Diamond’s et al [ 5 ] dataset, which comprises reference sequences from Quiza et al [ 18 ] (Table S12, Additional file 18 and Data S6, Additional file 19 ).…”

“…Custom-made HMMs targeting nitrite oxidoreductase subunits A and B (NxrA and NxrB), periplasmic cytochrome c nitrite reductase (NirS, cd1-NIR heme-containing), cytochrome c -dependent nitric oxide reductase (NorC; cNOR), hydrazine dehydrogenase (HzoA), hydrazine synthase (HzsA), dissimilatory sulfite reductase D (DsrD), sulfide:quinone reductase (Sqr), sulfur dioxygenase (Sdo), ribulose-bisphosphate carboxylase (RuBisCO) form I and form II, and alcohol dehydrogenases (Pqq-XoxF-MxaF) were obtained from Anantharaman et al [ 7 ]. NiFe and FeFe hydrogenases were predicted using HMMs from Méheust et al [ 47 ] and assigned to functional groups following Matheus Carnevali et al [ 38 ] (see Phylogenetic analyses subsection below for tree construction methods; Data S3, Additional file 12 and Data S4, Additional file 13 ; Table S9, Additional file 14 and Table S10, Additional file 15 ). No real group 4 membrane-bound NiFe hydrogenases were identified among the East River representative genomes (data not shown).…”

Bacterial and Archaeal Diversity and Abundance in Shallow Subsurface Clay Sediments at Jianghan Plain, China

“…Furthermore, Bathyarchaeota itself in the bottom clay layers might also have a potential of methanogenesis, which was supported by methane metabolism found in Bathyarchaeota genomes (BA1 and BA2) recovered from a deep aquifer (Evans et al, 2015;Lloyd, 2015). Elusimicrobia, another microbial population appearing in bottom samples A5 and A6 (Figure 4), might contribute to various substrates for methanogens by sugar fermentation to acetate, malate and butyrate, suggested by recent reconstructed Elusimicrobia genomes analysis from groundwater and other natural environments (Meheust et al, 2020). Beyond methanogenesis, these fermentation products could also to be used by the members in class Dehalococcoidia residing in bottom samples A5 and A6 ( Figure 4B) to respire the organohalide, a widespread recalcitrant pollutant in groundwater systems (Yang et al, 2020).…”