Multiple origins of anaerobic ciliates with hydrogenosomes within the radiation of aerobic ciliates

Abstract

Some ciliates live anaerobically and lack mitochondria, but possess hydrogenosomes: organelles that contain hydrogenase and produce hydrogen. The origin of hydrogenosomes has been explained by two competing hypotheses: (i) they are biochemically modified mitochondria; or (ii) they are derived from endosymbiotic association(s) of ciliates and anaerobic eubacteria that possessed the hydrogenosome biochemistry. Phylogenetic analyses of representative aerobic, and anaerobic hydrogenosomal ciliates using host nuclear SSU rDNA sequences indicate a minimum of three, but more likely four, separate origins of hydrogenosomes. Whereas this does not refute either hypothesis, the implausibility of multiple convergent endosymbioses gives further support to the view that hydrogenosomes in ciliates derive from an existing organelle, which ultrastructural evidence suggests is the mitochondrion. Our results indicate a considerable potential for physiological-biochemical plasticity among a group of predominantly aerobic eucaryotes, and provide a phylogenetic framework to further refine and test hypotheses of the origins of the hydrogenosomal enzymes.

Large-scale phylogenomic analysis reveals the phylogenetic position of the problematic taxon Protocruzia and unravels the deep phylogenetic affinities of the ciliate lineages

“…The ciliate tree is divided in two deep lineages -the Postciliodesmatophora and Intramacronucleata, a split that is supported by both molecular and morphological lines of evidence (BaroinTourancheau et al, 1998;Embley et al, 1995;Gao et al, 2010;Hirt et al, 1995;Lynn, 1996Lynn, , 2003. Beyond this deep division, it is generally agreed that there are 11 major ciliate lineages or classes and a twelfth single species clade of Cariacotrichea (Adl et al, 2012;Lynn, 2008;Orsi et al, 2012;Stoeck et al, 2003).…”

“…Beyond this deep division, it is generally agreed that there are 11 major ciliate lineages or classes and a twelfth single species clade of Cariacotrichea (Adl et al, 2012;Lynn, 2008;Orsi et al, 2012;Stoeck et al, 2003). Most of these classes are strongly supported by morphology, with the exception of the ''riboclasses'' -the Armophorea and Plagiopylea, which are identified only by sequences of the 18S rRNA genes, as included taxa lack any morphological synapomorphies (Bernhard et al, 1995(Bernhard et al, , 2001Cameron et al, 2001;Embley et al, 1995;Greenwood et al, 1991;Leipe et al, 1994;Lynn, 2008;Lynn et al, 1999;Lynn and Strüder-Kypke, 2002;Snoeyenbos-West et al, 2004;Stechmann et al, 1998). Nevertheless, the monophyly of the class Spirotrichea has been challenged in several studies, notably those that include Protocruzia spp.…”

Hydrogenosomes in the anaerobic fungus Neocallimastix frontalis have a double membrane but lack an associated organelle genome

“…The paucity of data has made it difficult to infer the relationships between these organelles and those occurring in trichomonads and anaerobic ciliates. Because hydrogenosomes are found in a broad phylogenetic range of amitochondriate organisms [2-A] it has been suggested that they must have been acquired independently [4]. Hydrogenosomes are a site of substrate-level phosphorylation and are significant energetically for these taxa.…”

“…Fax: (31) suggested that hydrogenosomes in anaerobic ciliates and trichomonads are derived from mitochondria [5]. In contrast, fungal hydrogenosomes have been reported to possess only a single membrane [6] giving rise to the hypothesis that microbodies are the progenitor organelles for these particular hydrogenosomes [4,[6][7][8].…”

“…In Trichomonas vaginalis and Tritrichomonas foetus the possibility of an associated organelle genome has been explored with little success, although the results are not conclusive [9,10]. The potential loss of a genome has been explained by loss of aerobic functions encoded by the genome rendering it redundant [4]. The presence of a genome would of course allow more direct tests of possible endosymbiotic origins.…”