Deianiraea, an extracellular bacterium associated with the ciliate Paramecium, suggests an alternative scenario for the evolution of Rickettsiales

Abstract

Rickettsiales are a lineage of obligate 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 synthesise 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 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.

SeqDeχ: A Sequence Deconvolution Tool for Genome Separation of Endosymbionts From Mixed Sequencing Samples

“…Symbionts have often evolved for long time in an environment endowed with a very peculiar fitness landscape; this translates in their usually divergent genomic properties (extremely reduced gene content, AT richness, etc.). Furthermore, we are only scratching at the surface of the diversity of existing symbionts, and very often the study of novel symbionts leads to the discovery of novel genera or even families (Castelli et al, 2019). For the above reasons, the taxonomy assignment based on blast generally leads to relatively few contigs being labeled.…”

When bacteria meet mitochondria: The strange case of the tick symbiont Midichloria mitochondrii †

“…Midichloria is a genus of obligate intracellular bacteria belonging to the order Rickettsiales, a group of alphaproteobacteria composed by intracellular bacteria (with one exception; Castelli et al, 2019), which includes human pathogens (e.g. many Rickettsia species; Parola et al, 2013;Weinert, Werren, Aebi, Stone, & Jiggins, 2009), mutualists (Hosokawa, Koga, Kikuchi, Meng, & Fukatsu, 2010;Landmann, 2019;Taylor, Bandi, & Hoerauf, 2005), reproductive parasites (Werren, Baldo, & Clark, 2008) and a number of less-studied lineages with unknown interactions with their host (Castelli, Sassera, & Petroni, 2016).…”

The Obligate Symbiont “Candidatus Megaira polyxenophila” Has Variable Effects on the Growth of Different Host Species

“…In 2013, a bacterial species of the order Rickettsiales has been described as endosymbiont of different ciliates (Schrallhammer et al, 2013). All members of this order are obligate intracellular bacteria hosted by eukaryotic organisms and strictly depend on their hosts for multiplication (Dumler et al, 2001) with the notable exception of the epibiont "Candidatus Deianiraea vastatrix" (Castelli et al, 2019a). "Candidatus Megaira polyxenophila" is remarkable as it has been found associated to potential hosts spanning a huge diversity, e.g., various ciliates (Sun et al, 2009;Vannini et al, 2005;Schrallhammer et al, 2013;Zaila et al, 2017), amoebae (Hess, 2017) chlorophytes and streptophytes (Hollants et al, 2013;Kawafune et al, 2015;Yang et al, 2016) and even cnidarians (Fraune and Bosch, 2007;Sunagawa et al, 2009).…”

“…Paramecium (Ciliophora, Oligohymenophorea) is a unicellular protist with a broad, nearly global distribution in fresh and brackish water bodies. This ciliate is studied, among other things ( Karunanithi et al, 2019 ; Kelz and Mashour, 2019 ; Mayne et al, 2019 ; Soares et al, 2019 ; Arnaiz et al, 2020 ) for the abundance and diversity of its endosymbionts ( Floriano et al, 2018 ; Garushyants et al, 2018 ; Grosser et al, 2018 ; Potekhin et al, 2018 ; Sabaneyeva et al, 2018 ; Schrallhammer et al, 2018 ; Castelli et al, 2019a , b ; Fokin et al, 2019 ; Koehler et al, 2019 ; Lanzoni et al, 2019 ; Plotnikov et al, 2019 ). Host-symbiont interactions and their outcome have been studied for example using Holospora ( Lohse et al, 2006 ; Hori et al, 2008 ; Fokin and Görtz, 2009 ; Nidelet et al, 2009 ; Duncan et al, 2013 , 2018 ; Banerji et al, 2015 ; Castelli et al, 2015 ; Dusi et al, 2015 ; Garushyants et al, 2018 ; Grosser et al, 2018 ) Caedibacter ( Kusch et al, 2002 ; Dusi et al, 2014 ; Grosser et al, 2018 ; Schu and Schrallhammer, 2018 ; Koehler et al, 2019 ) and Preeria ( Bella et al, 2016 ; Potekhin et al, 2018 ).…”