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Phylum Euglenozoa comprises three groups of eukaryotic microbes (kinetoplastids, diplonemids, and euglenids), the mitochondrial (mt) genomes of which exhibit radically different modes of organization and expression. Gene fragmentation is a striking feature of both euglenid and diplonemid mtDNAs. To rationalize the emergence of these highly divergent mtDNA types and the existence of insertion/deletion RNA editing (in kinetoplastids) and trans-splicing (in diplonemids), we propose that in the mitochondrion of the common evolutionary ancestor of Euglenozoa, small expressed gene fragments promoted a rampant neutral evolutionary pathway. Interactions between small antisense transcripts of these gene fragments and full-length transcripts, assisted by RNA-processing enzymes, permitted the emergence of RNA editing and/or trans-splicing activities, allowing the system to tolerate indel mutations and further gene fragmentation, respectively, and leading to accumulation of additional mutations. In this way, dramatically different mitochondrial genome structures and RNA-processing machineries were able to evolve. The paradigm of constructive neutral evolution acting on the widely different mitochondrial genetic systems in Euglenozoa posits the accretion of initially neutral molecular interactions by genetic drift, leading inevitably to the observed 'irremediable complexity'. [ABSTRACT FROM AUTHOR]

The euglenoids and kinetoplastids form a diverse assemblage of organisms which show no obvious phylogenetic relationship with other flagellates. An ultrastructural examination and comparison of the flagellar apparatus, the feeding apparatus, and mitotic nucleus indicate a number of shared morphological features which support a common ancestry for the two groups. Of particular interest is the euglenoid, Petalomonas cantuscygni, which shares many of the ultrastructural features common to both groups. Based on the data presented, we hypothesize that a euglenoid with features similar to those now present in P. cantuscygni was ancestral to both the euglenoid and kinetoplastid lines. [ABSTRACT FROM AUTHOR]