Euplotes magnicirratus (Ciliophora, Hypotrichia) depends on its bacterial endosymbiont 'Candidatus Devosia euplotis' for food digestion

Abstract

A symbiotic relationship between the marine ciliate Euplotes magnicirratus and an alpha-proteobacterium has recently been described. The bacterial symbiont, identified by molecular analysis as a new species of the genus Devosia, is referred to with the provisional name 'Candidatus Devosia euplotis'. This association is constant (it was found in different ciliate strains sampled in different geographical regions), and durable (it persisted in laboratory conditions for years). The physiological significance of this association was investigated through antibiotically produced aposymbiotic E. magnicirratus and attempts to grow the endosymbionts outside their host. Aposymbiotic protozoa completely lost the ability to digest the green alga Dunaliella tertiolecta, their usual food in laboratory conditions, and died. An investigation into the different steps of the digestive process showed that acidification of the digestive vacuoles occurred normally in both symbiotic and aposymbiotic ciliates, but that subsequent activation of acid phosphatase did not occur in aposymbiotic cells. Therefore, the ciliate depends on the symbiont for digestion of its green algal food and, as a consequence, for its survival. Attempts to grow bacterial endosymbionts on diluted culture media and on ciliate homogenate were unsuccessful. The results indicate that this represents a new type of symbiosis between prokaryotes and ciliates, which is mutualistic, and most likely obligatory for both partners.KEY WORDS: Alpha-proteobacteria · Ciliates · Devosia · Digestive process · Euplotes · Lysis · SymbiosisResale or republication not permitted without written consent of the publisher

NanoSIMS and tissue autoradiography reveal symbiont carbon fixation and organic carbon transfer to giant ciliate host

“…Phagotrophy in microzooids was already hypothesized based on ultrastructural observations of a fully developed digestive system and symbiont-like bacteria in the cytopharynx and inside digestive vacuoles (Bauer-Nebelsick et al, 1996b). In ciliates, ingested organisms observed in digestion vacuoles are not necessarily digested (Vannini et al, 2004). We therefore sought to detect acid phosphatase, an intracellular digestion marker, ultracytochemically (Holtzman, 1989).…”

Betaproteobacterial symbionts of the ciliate Euplotes: origin and tangled evolutionary path of an obligate microbial association

“…PCR reactions were performed using a ‘touchdown’ PCR (Don et al ., 1991), with the annealing taking place at 63°C, 57°C and 50°C. PCR products were then directly sequenced using internal primers (Vannini et al ., 2004) or cloned in a plasmid vector (pCR®2.1‐TOPO®, TOPO TA Cloning® Kit; Invitrogen, Carlsbad, CA, USA), inserted in chemically competent cells (One Shot TOP10®; Invitrogen) and used for libraries construction. In the case of libraries construction, three cloned inserts were sequenced and the consensus sequence was then used for the analysis (samples BB6, FAN10, EMP, PUHP, FL(12)‐VI).…”

Polynucleobacter Bacteria in the Brackish‐Water Species Euplotes harpa (Ciliata Hypotrichia)

“…In ciliates, as far as we know, a true dependence upon bacterial symbionts has been demonstrated only in Euplotes species harboring Polynucleobacter ‐like bacteria and in the marine species E. magnicirratus , harboring the newly identified α‐proteobacterial species “ Candidatus Devosia euplotis”. The latter ciliate is no longer able to digest food organisms once deprived of the symbiotic bacteria (Vannini et al 2004b). …”