TY - JOUR

T1 - ‘Candidatus Sarmatiella mevalonica’ endosymbiont of the ciliate Paramecium provides insights on evolutionary plasticity among Rickettsiales

AU - Castelli, Michele

AU - Lanzoni, Olivia

AU - Nardi, Tiago

AU - Lometto, Stefano

AU - Modeo, Letizia

AU - Potekhin, Alexey

AU - Sassera, Davide

AU - Petroni, Giulio

N1 - Funding Information: This work was funded by the University of Pisa PRA_2018_63 project to GP; the European Community's H2020 Programme H2020‐MSCA‐RISE 2019 grant 872767 to GP; the Italian Ministry of Education, University and Research (MIUR): Dipartimenti di Eccellenza Programme (2018–2022)—Department of Biology and Biotechnology ‘L. Spallanzani’, University of Pavia to DS; fluorescent and confocal microscopy observations were made possible with support of RSF grant 20‐14‐00220 to AP. The authors would like to thank A. Oren for advice in bacterial nomenclature, E. Gaucher and Y. Hoshino for providing alignments for mevalonate gene phylogenies, and S.S. Liu and L. Teng for providing genome sequence of endosymbiont of . Confocal microscopy was performed at the ‘Chromas’ Core Facility Center, Saint Petersburg State University, Russia. The WO2 culture is available upon a request from the RC CCM ‘Culture Collection of Microorganisms’, Saint Petersburg State University, Russia. Rickettsia Bemisia tabaci Publisher Copyright: © 2021 Society for Applied Microbiology and John Wiley & Sons Ltd. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/3

Y1 - 2021/3

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85099860854&partnerID=8YFLogxK

UR - https://www.mendeley.com/catalogue/35d93e95-01d9-31c8-b53f-11842fb6c8f2/

U2 - 10.1111/1462-2920.15396

DO - 10.1111/1462-2920.15396

M3 - Article

AN - SCOPUS:85099860854

VL - 23

SP - 1684

EP - 1701

JO - Environmental Microbiology

JF - Environmental Microbiology

SN - 1462-2912

IS - 3

ER -