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BMC Evolutionary Biology

, 9:287

First Online: 09 December 2009Received: 20 July 2009Accepted: 09 December 2009

Abstract

BackgroundHydrogenosomes are organelles that produce molecular hydrogen and ATP. The broad phylogenetic distribution of their hosts suggests that the hydrogenosomes of these organisms evolved several times independently from the mitochondria of aerobic progenitors. Morphology and 18S rRNA phylogeny suggest that the microaerophilic amoeboflagellate Psalteriomonas lanterna, which possesses hydrogenosomes and elusive -modified mitochondria-, belongs to the Heterolobosea, a taxon that consists predominantly of aerobic, mitochondriate organisms. This taxon is rather unrelated to taxa with hitherto studied hydrogenosomes.

ResultsElectron microscopy of P. lanterna flagellates reveals a large globule in the centre of the cell that is build up from stacks of some 20 individual hydrogenosomes. The individual hydrogenosomes are surrounded by a double membrane that encloses a homogeneous, dark staining matrix lacking cristae. The -modified mitochondria- are found in the cytoplasm of the cell and are surrounded by 1-2 cisterns of rough endoplasmatic reticulum, just as the mitochondria of certain related aerobic Heterolobosea. The ultrastructure of the -modified mitochondria- and hydrogenosomes is very similar, and they have the same size distribution as the hydrogenosomes that form the central stack.

The phylogenetic analysis of selected EST sequences Hsp60, Propionyl-CoA carboxylase supports the phylogenetic position of P. lanterna close to aerobic Heterolobosea Naegleria gruberi. Moreover, this analysis also confirms the identity of several mitochondrial or hydrogenosomal key-genes encoding proteins such as a Hsp60, a pyruvate:ferredoxin oxidoreductase, a putative ADP-ATP carrier, a mitochondrial complex I subunit 51 KDa, and a FeFe hydrogenase.

ConclusionComparison of the ultrastructure of the -modified mitochondria- and hydrogenosomes strongly suggests that both organelles are just two morphs of the same organelle. The EST studies suggest that the hydrogenosomes of P. lanterna are physiologically similar to the hydrogenosomes of Trichomonas vaginalis and Trimastix pyriformis. Phylogenetic analysis of the ESTs confirms the relationship of P. lanterna with its aerobic relative, the heterolobosean amoeboflagellate Naegleria gruberi, corroborating the evolution of hydrogenosomes from a common, mitochondriate ancestor.

Electronic supplementary materialThe online version of this article doi:10.1186-1471-2148-9-287 contains supplementary material, which is available to authorized users.

Rob M de Graaf, Isabel Duarte contributed equally to this work.

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Author: Rob M de Graaf - Isabel Duarte - Theo A van Alen - Jan WP Kuiper - Klaas Schotanus - Jörg Rosenberg - Martijn A Huynen

Source: https://link.springer.com/article/10.1186/1471-2148-9-287



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