A gene transfer event suggests a long-term partnership between eustigmatophyte algae and a novel lineage of endosymbiotic bacteria

Tatiana Yurchenko, Tereza Ševčíková, Pavel Přibyl, Khalid El Karkouri, Vladimír Klimeš, Raquel Amaral, Veronika Zbránková, Eunsoo Kim, Didier Raoult, Lilia M.A. Santos, Marek Eliáš

Research output: Contribution to journalArticlepeer-review

31 Scopus citations

Abstract

Rickettsiales are obligate intracellular bacteria originally found in metazoans, but more recently recognized as widespread endosymbionts of various protists. One genus was detected also in several green algae, but reports on rickettsialean endosymbionts in other algal groups are lacking. Here we show that several distantly related eustigmatophytes (coccoid algae belonging to Ochrophyta, Stramenopiles) are infected by Candidatus Phycorickettsia gen. nov., a new member of the family Rickettsiaceae. The genome sequence of Ca. Phycorickettsia trachydisci sp. nov., an endosymbiont of Trachydiscus minutus CCALA 838, revealed genomic features (size, GC content, number of genes) typical for other Rickettsiales, but some unusual aspects of the gene content were noted. Specifically, Phycorickettsia lacks genes for several components of the respiration chain, haem biosynthesis pathway, or c-di-GMP-based signalling. On the other hand, it uniquely harbours a six-gene operon of enigmatic function that we recently reported from plastid genomes of two distantly related eustigmatophytes and from various non-rickettsialean bacteria. Strikingly, the eustigmatophyte operon is closely related to the one from Phycorickettsia, suggesting a gene transfer event between the endosymbiont and host lineages in early eustigmatophyte evolution. We hypothesize an important role of the operon in the physiology of Phycorickettsia infection and a long-term eustigmatophyte-Phycorickettsia coexistence.

Original languageEnglish
Pages (from-to)2163-2175
Number of pages13
JournalISME Journal
Volume12
Issue number9
DOIs
StatePublished - 1 Sep 2018

Bibliographical note

Funding Information:
Acknowledgements We would like to thank Čestmír Vlček and Jan Pačes (Institute of Molecular genetics, Czech Academy of Sciences) and Pavel Flegontov (University of Ostrava) for their help with the assembly and validation of the Phycorickettsia genome sequence, Ashley Yang (American Museum of Natural History) for her assistance with TSA-FISH experiments, and Thomas Doak (Department of Biology, Indiana University, Bloomington) for sharing data prior to publication. This project has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement no. 642575. Further support for this work came from the Czech Science Foundation grant 17-21409S, the infrastructure grant „Přístroje IET“ (CZ.1.05/2.1.00/ 19.0388), and the project LO1208 of the National Feasibility Programme I of the Czech Republic. Access to computing and storage facilities owned by parties and projects contributing to the National Grid Infrastructure MetaCentrum, provided under the programme “Projects of Large Research, Development, and Innovations Infrastructures” (CESNET LM2015042), is greatly appreciated.

Publisher Copyright:
© 2018, International Society for Microbial Ecology.

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