Publications

3780

ABSTRACT The phylum Gemmatimonadota comprises mainly uncultured microorganisms that inhabit different environments such as soils, freshwater lakes, marine sediments, sponges, or corals. Based on 16S rRNA gene studies, the group PAUC43f is one of the most frequently retrieved Gemmatimonadota in marine samples. However, its physiology and ecological roles are completely unknown since, to date, not a single PAUC43f isolate or metagenome-assembled genome (MAG) has been characterized. Here, we carried out a broad study of the distribution, abundance, ecotaxonomy, and metabolism of PAUC43f, for which we propose the name of Palauibacterales . This group was detected in 4,965 16S rRNA gene amplicon datasets, mainly from marine sediments, sponges, corals, soils, and lakes, reaching up to 34.3% relative abundance, which highlights its cosmopolitan character, mainly salt-related. The potential metabolic capabilities inferred from 52 Palauibacterales MAGs recovered from marine sediments, sponges, and saline soils suggested a facultative aerobic and chemoorganotrophic metabolism, although some members may also oxidize hydrogen. Some Palauibacterales species might also play an environmental role as N 2 O consumers as well as suppliers of serine and thiamine. When compared to the rest of the Gemmatimonadota phylum, the biosynthesis of thiamine was one of the key features of the Palauibacterales . Finally, we show that polysaccharide utilization loci (PUL) are widely distributed within the Gemmatimonadota so that they are not restricted to Bacteroidetes , as previously thought. Our results expand the knowledge about this cryptic phylum and provide new insights into the ecological roles of the Gemmatimonadota in the environment. IMPORTANCE Despite advances in molecular and sequencing techniques, there is still a plethora of unknown microorganisms with a relevant ecological role. In the last years, the mostly uncultured Gemmatimonadota phylum is attracting scientific interest because of its widespread distribution and abundance, but very little is known about its ecological role in the marine ecosystem. Here we analyze the global distribution and potential metabolism of the marine Gemmatimonadota group PAUC43f, for which we propose the name of Palauibacterales order. This group presents a saline-related character and a chemoorganoheterotrophic and facultatively aerobic metabolism, although some species might oxidize H 2 . Given that Palauibacterales is potentially able to synthesize thiamine, whose auxotrophy is the second most common in the marine environment, we propose Palauibacterales as a key thiamine supplier to the marine communities. This finding suggests that Gemmatimonadota could have a more relevant role in the marine environment than previously thought.

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 subterranean world hosts up to one-fifth of all biomass, including microbial communities that drive transformations central to Earth’s biogeochemical cycles. However, little is known about how complex microbial communities in such environments are structured, and how inter-organism interactions shape ecosystem function. Here we apply terabase-scale cultivation-independent metagenomics to aquifer sediments and groundwater, and reconstruct 2,540 draft-quality, near-complete and complete strain-resolved genomes that represent the majority of known bacterial phyla as well as 47 newly discovered phylum-level lineages. Metabolic analyses spanning this vast phylogenetic diversity and representing up to 36% of organisms detected in the system are used to document the distribution of pathways in coexisting organisms. Consistent with prior findings indicating metabolic handoffs in simple consortia, we find that few organisms within the community can conduct multiple sequential redox transformations. As environmental conditions change, different assemblages of organisms are selected for, altering linkages among the major biogeochemical cycles.

The potential metabolism and ecological roles of many microbial taxa remain unknown because insufficient genomic data are available to assess their functional potential. Two such microbial “dark matter” taxa are the Candidatus bacterial phyla Cloacimonadota and Omnitrophota, both of which have been identified in global anoxic environments, including (but not limited to) organic-carbon-rich lakes. Using 24 metagenome-assembled genomes (MAGs) obtained from an Antarctic lake (Ace Lake, Vestfold Hills), novel lineages and novel metabolic traits were identified for both phyla. The Cloacimonadota MAGs exhibited a capacity for carbon fixation using the reverse tricarboxylic acid cycle driven by oxidation of hydrogen and sulfur. Certain Cloacimonadota MAGs encoded proteins that possess dockerin and cohesin domains, which is consistent with the assembly of extracellular cellulosome-like structures that are used for degradation of polypeptides and polysaccharides. The Omnitrophota MAGs represented phylogenetically diverse taxa that were predicted to possess a strong biosynthetic capacity for amino acids, nucleosides, fatty acids, and essential cofactors. All of the Omnitrophota were inferred to be obligate fermentative heterotrophs that utilize a relatively narrow range of organic compounds, have an incomplete tricarboxylic acid cycle, and possess a single hydrogenase gene important for achieving redox balance in the cell. We reason that both Cloacimonadota and Omnitrophota form metabolic interactions with hydrogen-consuming partners (methanogens and Desulfobacterota, respectively) and, therefore, occupy specific niches in Ace Lake.

Enterococci are gut microbes of most land animals. Likely appearing first in the guts of arthropods as they moved onto land, they diversified over hundreds of millions of years adapting to evolving hosts and host diets. Over 60 enterococcal species are now known. Two species, Enterococcus faecalis and Enterococcus faecium, are common constituents of the human microbiome. They are also now leading causes of multidrug-resistant hospital-associated infection. The basis for host association of enterococcal species is unknown. To begin identifying traits that drive host association, we collected 886 enterococcal strains from widely diverse hosts, ecologies, and geographies. This identified 18 previously undescribed species expanding genus diversity by >25%. These species harbor diverse genes including toxins and systems for detoxification and resource acquisition. Enterococcus faecalis and E. faecium were isolated from diverse hosts highlighting their generalist properties. Most other species showed a more restricted distribution indicative of specialized host association. The expanded species diversity permitted the Enterococcus genus phylogeny to be viewed with unprecedented resolution, allowing features to be identified that distinguish its four deeply rooted clades, and the entry of genes associated with range expansion such as B-vitamin biosynthesis and flagellar motility to be mapped to the phylogeny. This work provides an unprecedentedly broad and deep view of the genus Enterococcus , including insights into its evolution, potential new threats to human health, and where substantial additional enterococcal diversity is likely to be found.

The International Code of Nomenclature of Prokaryotes (ICNP) recently underwent some major modifications regarding the higher taxonomic ranks. On the one hand, the phylum category was introduced into the ICNP, which rapidly led to the valid publication of more than forty names of phyla. On the other hand, a decision on the retroactivity of Rule 8 regarding the names of classes was made, which removed most of the nomenclatural uncertainty that had affected those names during the last decade. However, it turned out that a number of names at the ranks of class, order and family are either not validly published or are validly published but illegitimate, although these names occur in the literature and are based on the type genus of a phylum with a validly published name. A closer examination of the literature for these and similar cases indicates that the names are unavailable under the ICNP either because of minor formal errors in the original descriptions, because another name should have been adopted for the taxon when the name was proposed, because of taxonomic uncertainties that were settled in the meantime, or because the names were placed on the list of rejected names. The purpose of this article is to fill the gaps by providing the missing formal descriptions and to ensure that the resulting taxon names are attributed to the original authors who did the taxonomic work.

AbstractTrace metals have been an important ingredient for life throughout Earth’s history. Here, we describe the genome-guided cultivation of a member of the elusive archaeal lineage Caldarchaeales (syn. Aigarchaeota), Wolframiiraptor gerlachensis, and its growth dependence on tungsten. A metagenome-assembled genome (MAG) of W. gerlachensis encodes putative tungsten membrane transport systems, as well as pathways for anaerobic oxidation of sugars probably mediated by tungsten-dependent ferredoxin oxidoreductases that are expressed during growth. Catalyzed reporter deposition-fluorescence in-situ hybridization (CARD-FISH) and nanoscale secondary ion mass spectrometry (nanoSIMS) show that W. gerlachensis preferentially assimilates xylose. Phylogenetic analyses of 78 high-quality Wolframiiraptoraceae MAGs from terrestrial and marine hydrothermal systems suggest that tungsten-associated enzymes were present in the last common ancestor of extant Wolframiiraptoraceae. Our observations imply a crucial role for tungsten-dependent metabolism in the origin and evolution of this lineage, and hint at a relic metabolic dependence on this trace metal in early anaerobic thermophiles.