The metabolic capacity, stress response and evolution of uncultured environmental Tenericutes have remained elusive, since previous studies have been largely focused on pathogenic species. In this ...study, we expanded analyses on Tenericutes lineages that inhabit various environments using a collection of 840 genomes.
Several environmental lineages were discovered inhabiting the human gut, ground water, bioreactors and hypersaline lake and spanning the Haloplasmatales and Mycoplasmatales orders. A phylogenomics analysis of Bacilli and Tenericutes genomes revealed that some uncultured Tenericutes are affiliated with novel clades in Bacilli, such as RF39, RFN20 and ML615. Erysipelotrichales and two major gut lineages, RF39 and RFN20, were found to be neighboring clades of Mycoplasmatales. We detected habitat-specific functional patterns between the pathogenic, gut and the environmental Tenericutes, where genes involved in carbohydrate storage, carbon fixation, mutation repair, environmental response and amino acid cleavage are overrepresented in the genomes of environmental lineages, perhaps as a result of environmental adaptation. We hypothesize that the two major gut lineages, namely RF39 and RFN20, are probably acetate and hydrogen producers. Furthermore, deteriorating capacity of bactoprenol synthesis for cell wall peptidoglycan precursors secretion is a potential adaptive strategy employed by these lineages in response to the gut environment.
This study uncovers the characteristic functions of environmental Tenericutes and their relationships with Bacilli, which sheds new light onto the pathogenicity and evolutionary processes of Mycoplasmatales.
Summary
The low temperature and elevated hydrostatic pressure in hadal trenches at water depths below 6000 m render sample collection difficult. Here, in situ hadal water microbial samples were ...collected from the Mariana Trench and analysed. The hadal microbial communities at different depths were revealed to be consistent and were dominated by heterotrophic Marinimicrobia. Thirty high‐quality metagenome‐assembled genomes (MAGs) were retrieved to represent the major hadal microbes affiliated with 12 prokaryotic phyla. Most of the MAGs were newly reported and probably derived from novel hadal inhabitants as exemplified by a potentially new candidate archaeal phylum in the DPANN superphylum. Metabolic reconstruction indicated that a great number of the MAGs participated in nitrogen and sulfur cycling, in which the nitrification process was driven sequentially by Thaumarchaeota and Nitrospirae and sulfur oxidization by Rhodospirillales in the Alphaproteobacteria class. Moreover, several groups of hadal microbes were revealed to be potential carbon monoxide oxidizers. Metatranscriptomic result highlighted the contribution of Chloroflexi in degrading recalcitrant dissolved organic matter and Marinimicrobia in extracellular protein decomposition. The present work provides an in‐depth view on the hadal microbial communities regarding their endemism and element cycles.
Summary
Various lineages of ammonia‐oxidizing archaea (AOA) are present in deep waters, but the mechanisms that determine ecotype formation are obscure. We studied 18 high‐quality genomes of the ...marine group I AOA lineages (alpha, gamma and delta) from the Mariana and Ogasawara trenches. The genomes of alpha AOA resembled each other, while those of gamma and delta lineages were more divergent and had even undergone insertion of some phage genes. The instability of the gamma and delta AOA genomes could be partially due to the loss of DNA polymerase B (polB) and methyladenine DNA glycosylase (tag) genes responsible for the repair of point mutations. The alpha AOA genomes harbour genes encoding a thrombospondin‐like outer membrane structure that probably serves as a barrier to gene flow. Moreover, the gamma and alpha AOA lineages rely on vitamin B12‐independent MetE and B12‐dependent MetH, respectively, for methionine synthesis. The delta AOA genome contains genes involved in uptake of sugar and peptide perhaps for heterotrophic lifestyle. Our study provides insights into co‐occurrence of cladogenesis and anagenesis in the formation of AOA ecotypes that perform differently in nitrogen and carbon cycling in dark oceans.
Protective symbiosis has been reported in many organisms, but the molecular mechanisms of the mutualistic interactions between the symbionts and their hosts are unclear. Here, we sequenced the ...424-kbp genome of "
Spiroplasma holothuricola," which dominated the hindgut microbiome of a sea cucumber, a major scavenger captured in the Mariana Trench (6,140 m depth). Phylogenetic relationships indicated that the dominant bacterium in the hindgut was derived from a basal group of
species. In this organism, the genes responsible for the biosynthesis of amino acids, glycolysis, and sugar transporters were lost, strongly suggesting endosymbiosis. The highly decayed genome consists of two chromosomes and harbors genes coding for proteolysis, microbial toxin, restriction-methylation systems, and clustered regularly interspaced short palindromic repeats (CRISPRs), composed of three
genes and 76 CRISPR spacers. The holothurian host is probably protected against invading viruses from sediments by the CRISPRs/Cas and restriction systems of the endosymbiotic spiroplasma. The protective endosymbiosis indicates the important ecological role of the ancient
symbiont in the maintenance of hadal ecosystems.
Sea cucumbers are major inhabitants in hadal trenches. They collect microbes in surface sediment and remain tolerant against potential pathogenic bacteria and viruses. This study presents the genome of endosymbiotic spiroplasmas in the gut of a sea cucumber captured in the Mariana Trench. The extreme reduction of the genome and loss of essential metabolic pathways strongly support its endosymbiotic lifestyle. Moreover, a considerable part of the genome was occupied by a CRISPR/Cas system to provide immunity against viruses and antimicrobial toxin-encoding genes for the degradation of microbes. This novel species of
is probably an important protective symbiont for the sea cucumbers in the hadal zone.
Deep‐sea isopod scavengers such as Bathynomus sp. are able to live in nutrient‐poor environments, which is likely attributable to the presence of symbiotic microbes in their stomach. In this study we ...recovered two draft genomes of mycoplasmas, Bg1 and Bg2, from the metagenomes of the stomach contents and stomach sac of a Bathynomus sp. sample from the South China Sea (depth of 898 m). Phylogenetic trees revealed a considerable genetic distance to other mycoplasma species for Bg1 and Bg2. Compared with terrestrial symbiotic mycoplasmas, the Bg1 and Bg2 genomes were enriched with genes encoding phosphoenolpyruvate‐dependent phosphotransferase systems (PTSs) and sodium‐driven symporters responsible for the uptake of sugars, amino acids and other carbohydrates. The genome of mycoplasma Bg1 contained sialic acid lyase and transporter genes, potentially enabling the bacteria to attach to the stomach sac and obtain organic carbons from various cell walls. Both of the mycoplasma genomes contained multiple copies of genes related to proteolysis and oligosaccharide degradation, which may help the host survive in low‐nutrient conditions. The discovery of the different types of mycoplasma bacteria in the stomach of this deep‐sea isopod affords insights into symbiotic model of deep‐sea animals and genomic plasticity of mycoplasma bacteria.
Hadal trenches are characterized by not only high hydrostatic pressure but also scarcity of nutrients and high diversity of viruses. Snailfishes, as the dominant vertebrates, play an important role ...in hadal ecology. Although studies have suggested possible reasons for the tolerance of hadal snailfish to high hydrostatic pressure, little is known about the strategies employed by hadal snailfish to cope with low-nutrient and virus-rich conditions. In this study, the gut microbiota of hadal snailfish was investigated. A novel bacterium named "
Mycoplasma liparidae" was dominant in the guts of three snailfish individuals from both the Mariana and Yap trenches. A draft genome of "
Mycoplasma liparidae" was successfully assembled with 97.8% completeness by hybrid sequencing. A set of genes encoding riboflavin biosynthesis proteins and a clustered regularly interspaced short palindromic repeats (CRISPR) system was present in the genome of "
Mycoplasma liparidae," which was unusual for
. The functional repertoire of the "
Mycoplasma liparidae" genome is likely set to help the host in riboflavin supplementation and to provide protection against viruses via a super CRISPR system. Remarkably, genes encoding common virulence factors usually exist in Tenericutes pathogens but were lacking in the genome of "
Mycoplasma liparidae." All of these characteristics supported an essential role of "
Mycoplasma liparidae" in snailfish living in the hadal zone. Our findings provide further insights into symbiotic associations in the hadal biosphere.
Diffusing fluid at a deep-sea hydrothermal vent creates rapid, acute physico-chemical gradients that correlate strongly with the distribution of the vent fauna. Two alvinocaridid shrimps, Alvinocaris ...longirostris and Shinkaicaris leurokolos occupy distinct microhabitats around these vents and exhibit different thermal preferences. S. leurokolos inhabits the central area closer to the active chimney, while A. longirostris inhabits the peripheral area. In this study, we screened candidate genes that might be involved in niche separation and microhabitat adaptation through comparative transcriptomics. The results showed that among the top 20% of overexpressed genes, gene families related to protein synthesis and structural components were much more abundant in S. leurokolos compared to A. longirostris. Moreover, 15 out of 25 genes involved in cellular carbohydrate metabolism were related to trehalose biosynthesis, versus 1 out of 5 in A. longirostris. Trehalose, a non-reducing disaccharide, is a multifunctional molecule and has been proven to act as a protectant responsible for thermotolerance in Saccharomyces cerevisiae. Putative positively selected genes involved in chitin metabolism and the immune system (lectin, serine protease and antimicrobial peptide) were enriched in S. leurokolos. In particular, one collagen and two serine proteases were found to have experienced strong positive selection. In addition, sulfotransferase-related genes were both overexpressed and positively selected in S. leurokolos. Finally, genes related to structural proteins, immune proteins and protectants were overexpressed or positively selected. These characteristics could represent adaptations of S. leurokolos to its microhabitat, which need to be confirmed by more evidence, such as data from large samples and different development stages of these alvinocaridid shrimps.
Long inverted repeats (LIRs) are evolutionarily and functionally important structures in genomes because of their involvement in RNA interference, DNA recombination, and gene duplication. ...Identification of LIRs is highly complicated when mismatches and indels between the repeats are permitted. Long inverted repeat explorer (Lirex) was developed and introduced in this report. Written in Java, Lirex provides a user-friendly interface and allows users to specify LIR searching criteria, such as length of the region, as well as pattern and size of the repeats. Recombinogenic LIRs can be selected on the basis of mismatch rate and internal spacer size from identified LIRs. Lirex, as a cross-platform tool to identify LIRs in a genome, may assist in designing following experiments to explore the function of LIRs. Our tool can identify more LIRs than other LIR searching tools. Lirex is publicly available at http://124.16.219.129/Lirex.
SAR202 in Chloroflexi phylum plays an important role in degradation of organic compounds in the oligotrophic deep ocean. Due to lack of high-quality genomes from across all depths of the water ...column, the metabolic capacities of the SAR202 subclusters in the marine environment were still largely unknown. In this study, we discovered the dynamics of the SAR202 subclusters in vertical layers of global ocean. A total of 11 metagenome-assembled genomes (MAGs) in various sizes were obtained from two SAR202 subclusters in the Mariana Trench. Genomic comparison revealed that vitamin B12 (VB12) synthesis was restricted to the subcluster III. In addition, the presence of a large number of genes encoding the oxidase and degradation pathways indicates that the SAR202 bacteria are probably capable of metabolizing chitin, aromatic compounds, dimethyl sulfoxide and osmolytes in the environment. With the predicted genes responsible for sulfite oxidation and export, SAR202 could potentially play important roles in biogeochemical cycles. This study highlights the genetic plasticity and ecological role of SAR202 in deep-sea zones.
•We discovered the ubiquitous distribution and the dynamics of the SAR202 subclusters in vertical layers of global ocean.•11 genomes were obtained for SAR202 subclusters in the Mariana Trench, which provided in-depth understanding of their metabolic capacities.•Genomics of deep-sea samples casts lights on the mechanisms that foster the diversification of the SAR202 subclusters and ecotypes.
Marinimicrobia are widespread from the marine surface to the hadal zone. Major clades of Marinimicrobia have evolved to different ecotypes along with energy gradients, but their genomes in deeper ...waters and sediments have rarely been studied. Here we obtained 11 Marinimicrobia draft genomes from the water column in the full-ocean depth and the hadal sediments in the Mariana Trench. All the predicted genomic capabilities of the metagenome-assembled genomes (MAGs) are indicative of heterotrophic lifestyle. The MAGs from the hadal depths are distinct from those from the mesopelagic and bathypelagic depths by enrichment of the genes involved in amino acids metabolism and mismatch repair. Compared with the MAGs from waters, those from the sediments were dramatically expanded by acquiring the genes responsible for chemotaxis, mobility and the two-component systems. Marinimicrobia were apparently differentiated in the environments with different depths, organic matters and electronic acceptors. Our results also posit a potential evolutionary relationship between the species inhabiting the waters and sediments, indicating the occurrence of allopatric speciation in Marinimicrobia.
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