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

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.

Eukaryotic Acquisition of a Bacterial Operon

“…Portions of the genome of an intracellular bacterial endosymbiont of insects have been found in insect genomes, with the transferred chunks ranging in size from roughly 500 bp to nearly the entire endosymbiont genome (Kondo et al, 2002;Nikoh et al, 2008;Dunning Hotopp et al, 2007). Furthermore, the plastid genomes of some eustigmatophyte algae harbor an operon of bacterial origin, although the function of the transferred genes in this case is uncertain (Yurchenko et al, 2016(Yurchenko et al, , 2018. A two-gene operon of archaeal origin was discovered in the protist Pygsuia nuclear genome, but these genes were subsequently fused into a single open reading frame (ORF) (Stairs et al, 2014).…”

The extracellular association of the bacterium “CandidatusDeianiraea vastatrix” with the ciliateParameciumsuggests an alternative scenario for the evolution ofRickettsiales

“…In recent years, an increasing amount of research was produced on neglected members of the order Rickettsiales (e.g. Wang & Wu 2014;Martijn et al 2015;Schulz et al 2016;Szokoli et al 2016b;Castelli et al 2018;Floriano et al 2018;Yurchenko et al 2018), which, contrarily to those thoroughly studied in the past, are not of direct medical or veterinary concern. Such investigations represented a major contribution to understand the phylogenetic and genomic diversity of Rickettsiales, and are gradually reshaping our interpretation of their evolution.…”

Current bioeconomical interest in stramenopilic Eustigmatophyceae: a review

“…A recent study reported a new freshwater eustigmatophyte Forest Park Isolate 5 (FP5), which is able to shift the absorption of chlorophyll a to >705 nm and to grow under solely far-red light [156]. A new case of natural engineering with a novel lineage of endosymbiotic bacteria in eustigmatophyceans was discovered [157]. These authors also found a six-gene operon that possibly encodes a pathway which involves metabolites from both organisms resulting in an isoprenoid-cyclitol-derived compound, probably with antimicrobial or other protective activity.…”