Dataset Information

Complete Genome Sequence of "Candidatus Nanosynbacter" Strain HMT-348_TM7c-JB, a Member of Saccharibacteria Clade G1.

ABSTRACT: Saccharibacteria are abundant and diverse members of the human oral microbiome; however, they are poorly understood and appear to exhibit an epibiont/parasitic lifestyle dependent on host bacteria. Here, a complete metagenome-assembled genome (MAG) sequence of an organism from Saccharibacteria clade G1 human microbial taxon (HMT) 348 is reported, strain HMT-348_TM7c-JB.

SUBMITTER: Baker JL

PROVIDER: S-EPMC9119051 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Complete Genome Sequence of "Candidatus Nanosynbacter" Strain HMT-348_TM7c-JB, a Member of Saccharibacteria Clade G1.

Baker Jonathon L JL

Microbiology resource announcements 20220411 5

Saccharibacteria are abundant and diverse members of the human oral microbiome; however, they are poorly understood and appear to exhibit an epibiont/parasitic lifestyle dependent on host bacteria. Here, a complete metagenome-assembled genome (MAG) sequence of an organism from Saccharibacteria clade G1 human microbial taxon (HMT) 348 is reported, strain HMT-348_TM7c-JB. ...[more]

PMID: 35404101

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Project description:Saccharibacteria Nanosynbacter lyticus strain TM7x is a member of the broadly distributed candidate phylum radiation. These bacteria have ultrasmall cell sizes, have reduced genomes, and live as epibionts on the surfaces of other bacteria. The mechanisms by which they establish and maintain this relationship are not yet fully understood. The transcriptomes of the epibiont TM7x and its host bacteria Schaalia odontolytica strain XH001 were captured across the establishment of symbiosis during both the initial interaction and stable symbiosis. The results showed a dynamic interaction with large shifts in gene expression for both species between the initial encounter and stable symbiosis, notably in transporter genes. During stable symbiosis, the host XH001 showed higher gene expression for peptidoglycan biosynthesis, mannosylation, cell cycle and stress-related genes, whereas it showed lower expression of chromosomal partitioning genes. This was consistent with the elongated cell shape seen in XH001 infected with TM7x and our discovery that infection resulted in thickened cell walls. Within TM7x, increased pili, type IV effector genes, and arginine catabolism/biosynthesis gene expression during stable symbiosis implied a key role for these functions in the interaction. Consistent with its survival and persistence in the human microbiome as an obligate epibiont with reduced de novo biosynthetic capacities, TM7x also showed higher levels of energy production and peptidoglycan biosynthesis, but lower expression of stress-related genes, during stable symbiosis. These results imply that TM7x and its host bacteria keep a delicate balance in order to sustain an episymbiotic lifestyle. IMPORTANCE Nanosynbacter lyticus type strain TM7x is the first cultivated member of the Saccharibacteria and the candidate phyla radiation (CPR). It was discovered to be ultrasmall in cell size with a highly reduced genome that establishes an obligate epibiotic relationship with its host bacterium. The CPR is a large, monophyletic radiation of bacteria with reduced genomes that includes Saccharibacteria. The vast majority of the CPR have yet to be cultivated, and our insights into these unique organisms to date have been derived from only a few Saccharibacteria species. Being obligate parasites, it is unknown how these ultrasmall Saccharibacteria, which are missing many de novo biosynthetic pathways, are maintained at a high prevalence within the human microbiome as well as in the environment.

Project description:The ultra-small, obligate parasitic epibiont, TM7x, the first and only current member of the long-elusive Saccharibacteria (formerly the TM7 phylum) phylum to be cultivated, was isolated in co-culture with its bacterial host, Actinomyces odontolyticus subspecies actinosynbacter, XH001. Initial phenotypic characterization of the TM7x-associated XH001 co-culture revealed enhanced biofilm formation in the presence of TM7x compared to XH001 as monoculture. Genomic analysis and previously published transcriptomic profiling of XH001 also revealed the presence of a putative AI-2 quorum sensing (QS) operon, which was highly upregulated upon association of TM7x with XH001. This analysis revealed that the most highly induced gene in XH001 was an lsrB ortholog, which encodes a putative periplasmic binding protein for the auto inducer (AI)-2 QS signaling molecule. Further genomic analyses suggested the lsrB operon in XH001 is a putative hybrid AI-2/ribose transport operon as well as the existence of a luxS ortholog, which encodes the AI-2 synthase. In this study, the potential role of AI-2 QS in the epibiotic-parasitic relationship between XH001 and TM7x in the context of biofilm formation was investigated. A genetic system for XH001 was developed to generate lsrB and luxS gene deletion mutants in XH001. Phenotypic characterization demonstrated that deletion mutations in either lsrB or luxS did not affect XH001's growth dynamic, mono-species biofilm formation capability, nor its ability to associate with TM7x. TM7x association with XH001 induced lsrB gene expression in a luxS-dependent manner. Intriguingly, unlike wild type XH001, which displayed significantly increased biofilm formation upon establishing the epibiotic-parasitic relationship with TM7x, XH001ΔlsrB, and XH001ΔluxS mutants failed to achieve enhanced biofilm formation when associated with TM7x. In conclusion, we demonstrated a significant role for AI-2 QS in modulating dual-species biofilm formation when XH001 and TM7x establish their epibiotic-parasitic relationship.

Project description:Saccharibacteria (formerly TM7) have reduced genomes and a small cell size and appear to have a parasitic lifestyle dependent on a bacterial host. Although there are at least 6 major clades of Saccharibacteria inhabiting the human oral cavity, complete genomes of oral Saccharibacteria were previously limited to the G1 clade. In this study, nanopore sequencing was used to obtain three complete genome sequences from clade G6. Phylogenetic analysis suggested the presence of at least 3 to 5 distinct species within G6, with two discrete taxa represented by the 3 complete genomes. G6 Saccharibacteria were highly divergent from the more-well-studied clade G1 and had the smallest genomes and lowest GC content of all Saccharibacteria. Pangenome analysis showed that although 97% of shared pan-Saccharibacteria core genes and 89% of G1-specific core genes had putative functions, only 50% of the 244 G6-specific core genes had putative functions, highlighting the novelty of this group. Compared to G1, G6 harbored divergent metabolic pathways. G6 genomes lacked an F1Fo ATPase, the pentose phosphate pathway, and several genes involved in nucleotide metabolism, which were all core genes for G1. G6 genomes were also unique compared to that of G1 in that they encoded d-lactate dehydrogenase, adenylate cyclase, limited glycerolipid metabolism, a homolog to a lipoarabinomannan biosynthesis enzyme, and the means to degrade starch. These differences at key metabolic steps suggest a distinct lifestyle and ecological niche for clade G6, possibly with alternative hosts and/or host dependencies, which would have significant ecological, evolutionary, and likely pathogenic implications. IMPORTANCE Saccharibacteria are ultrasmall parasitic bacteria that are common members of the oral microbiota and have been increasingly linked to disease and inflammation. However, the lifestyle and impact on human health of Saccharibacteria remain poorly understood, especially for the clades with no complete genomes (G2 to G6) or cultured isolates (G2 and G4 to G6). Obtaining complete genomes is of particular importance for Saccharibacteria, because they lack many of the "essential" core genes used for determining draft genome completeness, and few references exist outside clade G1. In this study, complete genomes of 3 G6 strains, representing two candidate species, were obtained and analyzed. The G6 genomes were highly divergent from that of G1 and enigmatic, with 50% of the G6 core genes having no putative functions. The significant difference in encoded functional pathways is suggestive of a distinct lifestyle and ecological niche, probably with alternative hosts and/or host dependencies, which would have major implications in ecology, evolution, and pathogenesis.

Dataset Information

Complete Genome Sequence of "Candidatus Nanosynbacter" Strain HMT-348_TM7c-JB, a Member of Saccharibacteria Clade G1.

Publications

Complete Genome Sequence of "<i>Candidatus</i> Nanosynbacter" Strain HMT-348_TM7c-JB, a Member of <i>Saccharibacteria</i> Clade G1.

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