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Background  Microbial eukaryotes show large variations in genome structure and content between lineages, indicating extensive flexibility over evolutionary timescales. Here we address the tempo and mode of such changes within diplomonads, flagellated protists with two nuclei found in oxygen-poor environments. Approximately 5,000 expressed sequence tag (EST) sequences were generated from the fish commensal  Spironucleus barkhanus  and compared to sequences from the morphologically indistinguishable fish parasite  Spironucleus salmonicida , and other diplomonads. The ESTs were complemented with sequence variation studies in selected genes and genome size determinations.    Results  Many genes detected in  S. barkhanus  and  S. salmonicida  are absent in the human parasite  Giardia intestinalis , the most intensively studied diplomonad. For example, these fish diplomonads show an extended metabolic repertoire and are able to incorporate selenocysteine into proteins. The codon usage is altered in  S. barkhanus  compared to  S. salmonicida . Sequence variations were found between individual  S. barkhanus  ESTs for many, but not all, protein coding genes. Conversely, no allelic variation was found in a previous genome survey of  S. salmonicida . This difference was confirmed by sequencing of genomic DNA. Up to five alleles were identified for the cloned  S. barkhanus  genes, and at least nineteen highly expressed  S. barkhanus  genes are represented by more than four alleles in the EST dataset. This could be explained by the presence of a non-clonal  S. barkhanus  population in the culture, by a ploidy above four, or by duplications of parts of the genome. Indeed, genome size estimations using flow cytometry indicated similar haploid genome sizes in  S. salmonicida  and  G. intestinalis  (~12 Mb), whereas the  S. barkhanus  genome is larger (~18 Mb).    Conclusions  This study indicates extensive divergent genome evolution within diplomonads. Genomic traits such as codon usage, frequency of allelic sequence variation, and genome size have changed considerably between  S. barkhanus  and  S. salmonicida . These observations suggest that large genomic differences may accumulate in morphologically indistinguishable eukaryotic microbes.

Large genomic differences between the morphologically indistinguishable diplomonads Spironucleus barkhanus and Spironucleus salmonicida