Abstract
“Neglected Rickettsiaceae” (i.e. those harboured by non-hematophagous eukaryotic hosts) display greater phylogenetic variability and more widespread dispersal than pathogenic ones; yet, the knowledge about their actual host range and host shift mechanism is scarce. The present work reports the characterization following the full-cycle rRNA approach (SSU rRNA sequence, specific in situ hybridization, and ultrastructure) of a novel rickettsial bacterium, herewith proposed as 'Candidatus Megaira polyxenophila' gen. nov., sp. nov. We found it in association with four different free-living ciliates (Diophrys oligothrix, Euplotes octocarinatus, Paramecium caudatum, and Spirostomum sp., all belonging to Alveolata, Ciliophora); furthermore it was recently observed as intracellular occurring in Carteria cerasiformis and Pleodorina japonica (Chlorophyceae, Chlorophyta). Phylogenetic analyses demonstrated the belonging of the candidate new genus to the family Rickettsiaceae (Alphaproteobacteria, Rickettsiales) as a sister group of the genus Rickettsia. In situ observations revealed the ability of the candidate new species to colonize either nuclear or cytoplasmic compartments, depending on the host organism. The presence of the same bacterial species within different, evolutionary distant, hosts indicates that 'Candidatus Megaira polyxenophila' recently underwent several distinct host shifts, thus suggesting the existence of horizontal transmission pathways. We consider these findings as indicative of an unexpected spread of rickettsial infections in aquatic communities, possibly by means of trophic interactions, and hence propose a new interpretation of the origin and phylogenetic diversification of rickettsial bacteria.
Highlights
The family Rickettsiaceae (Alphaproteobacteria, Rickettsiales, [1]) comprises 28 validly described species, subdivided into the genera Rickettsia and Orientia
As far as all species comprised within the family Rickettsiaceae share an obligate intracellular lifestyle, we conjecture that the bacteria represented by those sequences are not free-living organisms occurring in the screened habitats but unrecognized endosymbionts
18 S rRNA gene data show 5 bp difference between the two strains and a similarity higher than 99% with other D. oligothrix sequences [47,48]. The morphology of this Spirostomum population 72 shared features with Spirostomum teres and, to a greater extent, with Spirostomum minus, but an unambiguous identification was not achieved. Molecular data placed this population closer to S. minus than to other species of the genus, but the differences in the SSU rRNA gene sequence did not support a clear identification of population 72 as S. minus
Summary
The family Rickettsiaceae (Alphaproteobacteria, Rickettsiales, [1]) comprises 28 validly described species, subdivided into the genera Rickettsia and Orientia (reviewed by [2]). The ‘‘neglected Rickettsiaceae’’, i.e. Rickettsia-like bacteria of less clinical concern, associated with non-hematophagous arthropods and/or with other eukaryotes, should be subject of considerable interest This group accounts for the main contribution to the evolutionary diversity of Rickettsiaceae, gathering 10 out of the 13 phylogenetic clusters comprised within that family (Fig. 1; [9]). These bacteria display a broad host range, including arthropods (reviewed by [11]), protists [12,13,14,15,16,17,18,19], cnidarians [20], leeches [21] and even plants [22,23], while medically relevant rickettsiae are typically confined to ticks or lice [2] with vertebrates as alternate hosts. This will allow at the same time to elucidate the evolutionary pattern of some typical rickettsial traits, such as the monoxenic or polyxenic life cycle and the development of pathogenic capabilities
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