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

Xuesong He, Jeffrey S. McLean, Anna Edlund, Shibu Yooseph, Adam P. Hall, Su Yang Liu, Pieter C. Dorrestein, Eduardo Esquenazi, Ryan C. Hunter, Genhong Cheng, Karen E. Nelson, Renate Lux, Wenyuan Shi

Research output: Contribution to journalArticlepeer-review

164 Scopus citations

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-innodataalpha 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.

Original languageEnglish (US)
Pages (from-to)244-249
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number1
DOIs
StatePublished - Jan 6 2015

Keywords

  • Epibiont
  • Human-associated
  • Interspecies interaction
  • Oral microbiome
  • TM7

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