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Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle.

ABSTRACT: The candidate phylum TM7 is globally distributed and often associated with human inflammatory mucosal diseases. Despite its prevalence, the TM7 phylum remains recalcitrant to cultivation, making it one of the most enigmatic phyla known. In this study, we cultivated a TM7 phylotype (TM7x) from the human oral cavity. This extremely small coccus (200-300 nm) has a distinctive lifestyle not previously observed in human-associated microbes. It is an obligate epibiont of an Actinomyces odontolyticus strain (XH001) yet also has a parasitic phase, thereby killing its host. This first completed genome (705 kb) for a human-associated TM7 phylotype revealed a complete lack of amino acid biosynthetic capacity. Comparative genomics analyses with uncultivated environmental TM7 assemblies show remarkable conserved gene synteny and only minimal gene loss/gain that may have occurred as TM7x adapted to conditions within the human host. Transcriptomic and metabolomic profiles provided the first indications, to our knowledge, that there is signaling interaction between TM7x and XH001. Furthermore, the induction of TNF-? production in macrophages by XH001 was repressed in the presence of TM7x, suggesting its potential immune suppression ability. Overall, our data provide intriguing insights into the uncultivability, pathogenicity, and unique lifestyle of this previously uncharacterized oral TM7 phylotype.

SUBMITTER: He X

PROVIDER: S-EPMC4291631 | biostudies-literature | 2015 Jan

REPOSITORIES: biostudies-literature

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Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle.

He Xuesong X McLean Jeffrey S JS Edlund Anna A Yooseph Shibu S Hall Adam P AP Liu Su-Yang SY Dorrestein Pieter C PC Esquenazi Eduardo E Hunter Ryan C RC Cheng Genhong G Nelson Karen E KE Lux Renate R Shi Wenyuan W

Proceedings of the National Academy of Sciences of the United States of America 20141222 1

The candidate phylum TM7 is globally distributed and often associated with human inflammatory mucosal diseases. Despite its prevalence, the TM7 phylum remains recalcitrant to cultivation, making it one of the most enigmatic phyla known. In this study, we cultivated a TM7 phylotype (TM7x) from the human oral cavity. This extremely small coccus (200-300 nm) has a distinctive lifestyle not previously observed in human-associated microbes. It is an obligate epibiont of an Actinomyces odontolyticus s ...[more]

PMID: 25535390

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Project description:Bacteriophages are considered the most abundant entities on earth. However, there are merely seven sequenced double-stranded RNA (dsRNA) phages, compared to thousands of sequenced double-stranded DNA (dsDNA) phages. Interestingly, dsRNA viruses are quite common in fungi and usually have a lifestyle of commensalism or mutualism. Thus, the classical protocol of using double-layer agar plates to characterize phage plaques might be significantly biased in the isolation of dsRNA phages beyond strictly lytic lifestyles. Thus, we applied a protocol for isolating fungal viruses to identify RNA phages in bacteria and successfully isolated a novel dsRNA phage, phiNY, from Microvirgula aerodenitrificans. phiNY has a genome consisting of three dsRNA segments, and its genome sequence has no nucleotide sequence similarity with any other phage. Although phiNY encodes a lytic protein of glycoside hydrolase, and phage particles are consistently released during bacterial growth, phiNY replication did not block bacterial growth, nor did it form any plaques on agar plates. More strikingly, the phiNY-infected strain grew faster than the phiNY-negative strain, indicating a mutualistic parasitic lifestyle. Thus, this study not only reveals a new mutualistic parasitic dsRNA phage but also implies that other virus isolation methods would be valuable to identify phages with nonlytic lifestyles. IMPORTANCE Viruses with dsRNA genomes are quite diverse and infect organisms in all three domains of life. Although dsRNA viruses that infect humans, plants, and fungi are quite common, dsRNA viruses that infect bacteria, known as bacteriophages, are quite understudied, and only seven dsRNA phages have been sequenced so far. One possible explanation for the rare isolation of dsRNA phages might be the protocol of the double-layer agar plate assay. Phages without strictly lytic lifestyles might not form plaques. Thus, we applied the protocol of isolating fungal viruses to identify RNA phages inside bacteria and successfully isolated a novel dsRNA phage, phiNY, with a mutualistic parasitic lifestyle. This study implies that dsRNA phages without strictly lytic lifestyles might be common in nature and deserve more investigations.

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Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle.

Publications

Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle.

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