4.6 Article

'Candidatus Sarmatiella mevalonica' endosymbiont of the ciliate Paramecium provides insights on evolutionary plasticity among Rickettsiales

期刊

ENVIRONMENTAL MICROBIOLOGY
卷 23, 期 3, 页码 1684-1701

出版社

WILEY
DOI: 10.1111/1462-2920.15396

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资金

  1. University of Pisa [PRA_2018_63]
  2. European Community's H2020 Programme H2020-MSCA-RISE 2019 grant [872767]
  3. Italian Ministry of Education, University and Research (MIUR): Dipartimenti di Eccellenza Programme (2018-2022)-Department of Biology and Biotechnology 'L. Spallanzani', University of Pavia
  4. RSF [20-14-00220]
  5. Russian Science Foundation [20-14-00220] Funding Source: Russian Science Foundation
  6. Marie Curie Actions (MSCA) [872767] Funding Source: Marie Curie Actions (MSCA)

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A newly discovered Rickettsiales bacterium associated with the ciliate Paramecium has a genome encoding lineage-specific features, particularly the mevalonate pathway gene repertoire. Additionally, phylogenetically unrelated mevalonate pathway genes were found in Rickettsiales sequences, suggesting evolutionary convergent effects of independent horizontal gene transfer events. This highlights convergence as an important evolutionary phenomenon in Rickettsiales, potentially contributing to hidden origins of nuanced similarities among sub-lineages.
Members of the bacterial order Rickettsiales are obligatorily associated with a wide range of eukaryotic hosts. Their evolutionary trajectories, in particular concerning the origin of shared or differential traits among distant sub-lineages, are still poorly understood. Here, we characterized a novel Rickettsiales bacterium associated with the ciliate Paramecium tredecaurelia and phylogenetically related to the Rickettsia genus. Its genome encodes significant lineage-specific features, chiefly the mevalonate pathway gene repertoire, involved in isoprenoid precursor biosynthesis. Not only this pathway has never been described in Rickettsiales, it also is very rare among bacteria, though typical in eukaryotes, thus likely representing a horizontally acquired trait. The presence of these genes could enable an efficient exploitation of host-derived intermediates for isoprenoid synthesis. Moreover, we hypothesize the reversed reactions could have replaced canonical pathways for producing acetyl-CoA, essential for phospholipid biosynthesis. Additionally, we detected phylogenetically unrelated mevalonate pathway genes in metagenome-derived Rickettsiales sequences, likely indicating evolutionary convergent effects of independent horizontal gene transfer events. Accordingly, convergence, involving both gene acquisitions and losses, is highlighted as a relevant evolutionary phenomenon in Rickettsiales, possibly favoured by plasticity and comparable lifestyles, representing a potentially hidden origin of other more nuanced similarities among sub-lineages.

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