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Open Access Research article

The hydrogenosomes of Psalteriomonas lanterna

Rob M de Graaf1, Isabel Duarte2, Theo A van Alen1, Jan WP Kuiper14, Klaas Schotanus15, Jörg Rosenberg3, Martijn A Huynen26 and Johannes HP Hackstein1*

Author Affiliations

1 Department of Evolutionary Microbiology, IWWR, Radboud University Nijmegen, Heyendaalseweg 135, 6525AJ Nijmegen, The Netherlands

2 Center for Molecular and Biomolecular Informatics, Nijmegen Center for Molecular Life Sciences, Radboud University Nijmegen Medical Centre, Geert Grooteplein 28, 6525GA Nijmegen, The Netherlands

3 Sommerhaus 45, D-50129 Bergheim, Germany

4 CIHR Group in Matrix Dynamics, University of Toronto, 150 College Street, Toronto, Ontario, Canada M5S 3E2

5 Department of Ecology and Evolutionary Biology, 106A Guyot Hall, Princeton University, Princeton NJ 08554-2016, USA

6 Netherlands Bioinformatic Centre, Geert Grooteplein 28, 6525 GA Nijmegen, The Netherlands

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BMC Evolutionary Biology 2009, 9:287  doi:10.1186/1471-2148-9-287

Published: 9 December 2009

Abstract

Background

Hydrogenosomes 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.

Results

Electron 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.

Conclusion

Comparison 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.