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

Abstract

Rickettsiales are a lineage of obligatorily intracellular Alphaproteobacteria, encompassing important human pathogens, manipulators of host reproduction, and mutualists. Here we report the discovery of a novel Rickettsiales bacterium associated with Paramecium, displaying a unique extracellular lifestyle, including the ability to replicate outside host cells. Genomic analyses show that the bacterium possesses a higher capability to synthesize amino acids, compared to all investigated Rickettsiales. Considering these observations, phylogenetic and phylogenomic reconstructions, and re-evaluating the different means of interaction of Rickettsiales bacteria with eukaryotic cells, we propose an alternative scenario for the evolution of intracellularity in Rickettsiales. According to our reconstruction, the Rickettsiales ancestor would have been an extracellular and metabolically versatile bacterium, while obligate intracellularity and genome reduction would have evolved later in parallel and independently in different sub-lineages. The proposed new scenario could impact on the open debate on the lifestyle of the last common ancestor of mitochondria within Alphaproteobacteria.

An updated phylogeny of the Alphaproteobacteria reveals that the parasitic Rickettsiales and Holosporales have independent origins

“…Hess et al, 2016; Montagna et al, 2013; Santos and Massard, 2014). It is exclusively composed of endosymbiotic bacteria living within diverse eukaryotes, and such a lifestyle is shared with all other members of the Rickettsiales (with the possible exception of a recently reported ectosymbiotic rickettialean; see Castelli et al, 2018). When we decrease, and then account for, compositional heterogeneity, we recover tree topologies in which the Holosporales moves away from the Rickettsiales (e.g.…”

Evolution ofWolbachiaMutualism and Reproductive Parasitism: Insight from Two Novel Strains that Co-infect Cat Fleas

“…Order Rickettsiales is a highly diverse group of obligate intracellular bacteria (2,62,90). A rapid pace of newly identified lineages (60,(91)(92)(93)(94)(95)(96)(97)(98)(99)(100)(101)(102)(103)(104) provides a rich source for evaluating mechanisms of evolution within constraints of the eukaryotic cell. Phage, plasmids, transposons, ICEs, and other insertion sequences are variably present across rickettsial genomes and mobilize numerous genes to offset reductive genome evolution and provide lifestyle altering traits (21).…”

Rickettsiales‐like organisms in bivalves and marine gastropods: a review

“…exhibit life cycles within trematodes that involve a series of aquatic hosts, including fish and insects (Yu & Walke 2006; Lawrence & Poulin, 2016). On the other hand, a great number of bacteria that are symbionts of ciliates belong to the order Rickettsiales , and these ciliates may play a role in the transmission of bacteria to other hosts (Castelli et al 2018). It must be emphasized here that comparisons of intracellular prokaryotic organisms found in molluscs with pathogenic or non‐pathogenic prokaryotes of the families Anaplasmataceae and Rickettsiaceae are based almost totally on morphological similarities.…”