Omnitrophota encompasses diverse and hyperactive nanobacteria: Potential metabolisms and host-dependent lifestyles

Abstract

Candidate bacterial phylum Omnitrophota has never been grown in axenic culture and is poorly understood. Here, we combined analysis of 421 Omnitrophota genomes representing six classes and 276 species and show that they are prevalent in water, sediments, and soils globally. Fluorescence-activated cell sorting and differential size filtration showed ultra-small (~0.2 μm) cells to be common across the phylum. Reduced genomes in all six classes maintained major biosynthetic and energy conservation pathways, particularly the acetogenic Wood-Ljungdahl pathway or diverse aerobic and anaerobic respirations. However, most genomes also encoded multiple systems typical of bacterial predators and intracellular parasites, suggesting possible predatory or parasitic lifestyles. In support of this, quantitative stable-isotope probing revealed three families with high isotope uptake rates comparable to obligate bacterial predators in diverse soils. Based on their ubiquity, small cell size, high metabolic activity, and genomic repertoire, many Omnitrophota are likely to be ecologically important in a wide range of ecosystems, possibly as predators or parasites.

A metagenomic view of novel microbial and metabolic diversity found within the deep terrestrial biosphere at DeMMO: A microbial observatory in South Dakota, USA

“…Putative fermentation and presence of genes for the Wood‐Ljungdahl pathway are highly abundant in Omnitrophota MAGs (Figure 5). The prevalence of the Wood‐Ljungdahl pathway in Omnitrophota genomes has been noted in other studies (Momper, Jungbluth, et al, 2017; Perez‐Molphe‐Montoya et al, 2022; Seymour, 2021; Seymour et al, 2023) and seems ubiquitous among the numerous clades of this candidate phylum, indicating an anaerobic and potentially mixotrophic lifestyle. Finally, analysis of D3_22, a high quality Eisenbacteria MAG, reveals that members of this candidate phylum may have highly diverse metabolic capabilities in DeMMO fluids, including nitrogen, sulfur, metal and oxygen transformation.…”

“…Members of the phylum Omnitrophota are particularly well represented in our dataset with MAGs originating from across DeMMO sites. The phylum was originally dubbed ‘Omnitrophica’ in 2013 (Rinke et al, 2013) and has received much attention in recent years, as they are a widespread and abundant candidate phylum in global natural environments such as sediment, non‐saline ground and surface water, and soils (Perez‐Molphe‐Montoya et al, 2022; Seymour, 2021; Seymour et al, 2023; Williams et al, 2022). Recent studies have posited that most Omnitrophota are ultra‐small nanobacteria (cell size <0.2 μm) and that they lead a symbiotic lifestyle (Seymour, 2021; Seymour et al, 2023).…”

“…The phylum was originally dubbed ‘Omnitrophica’ in 2013 (Rinke et al, 2013) and has received much attention in recent years, as they are a widespread and abundant candidate phylum in global natural environments such as sediment, non‐saline ground and surface water, and soils (Perez‐Molphe‐Montoya et al, 2022; Seymour, 2021; Seymour et al, 2023; Williams et al, 2022). Recent studies have posited that most Omnitrophota are ultra‐small nanobacteria (cell size <0.2 μm) and that they lead a symbiotic lifestyle (Seymour, 2021; Seymour et al, 2023). Although we did not investigate the potential for a symbiotic or predatory lifestyle, our metabolic analyses indicate that some Omnitrophota at DeMMO sites are likely capable of dissimilatory nitrite reduction to ammonia, sulfur oxidation, thiosulfate oxidation, and iron oxidation (Figure 5).…”

Microbial Assemblages and Metabolic Activity in Organic‐Rich Subterranean Estuaries: Impact of Climate and Land Use Changes

“…A previous study reported that Leptospirae, one of the taxa not found after the incubation, had difficulties multiplying following a microcosm experiment (Casanovas‐Massana et al., 2018). Another taxon, Omnitrophia, is known for its host‐dependent lifestyle (Seymour et al., 2022). It is likely that the altered environment during our incubation removed such hosts and lessened their survivability.…”

Comparison of Microbial Profiling and Tracer Testing for the Characterization of Injector-Producer Interwell Connectivities

“…The potential tendency for introduced microbial cells to be retained in porous/fractured media, on the other hand, highlights the abundant indigenous microbes that did transport out of the aquifer. A notable category of the produced-fluid members is, interestingly, those with documented ultrasmall body size, for example, members of the phyla Patescibacteria (also known as the Candidate Phyla Radiation or CPR) and Omnitrophicaeota (also known as Omnitrophota, Omnitrophica or OP3) [67,68], both of which still lack culturable representatives, yet were found to be prevalent in oligotrophic groundwater environments worldwide in high abundance [25,[67][68][69]. Among the 50 samples in this study, members of the Patescibacteria and Omnitrophicaeota phyla were prevalent and constituted up to 39.3% and 16.1% of the produced communities, respectively.…”