Genetic diversity of goniomonads: an ancient divergence between marine and freshwater species

Abstract

Goniomonas is a ubiquitous free-living, phagotrophic zooflagellate genus related to the photosynthetic cryptophytes. Only one freshwater and two marine species have been described. Although the two marine species (G. pacifica and G. amphinema) are morphologically quite distinct from each other, it was unclear until recently whether one of them (G. pacifica) is really separate from the freshwater G. truncata because their morphology and size are so similar. We have isolated six new Goniomonas strains and amplified and sequenced their small subunit ribosomal RNA genes. Our results reveal remarkable genetic diversity within all three nominal species and confirm that G. pacifica is genetically very distinct from G. truncata. Within each morphospecies there is more divergence than between many cryptophyte genera and there are many more substantially different genotypes of Goniomonas than established 'species'. This implies that there are numerous undescribed 'species' of Goniomonas and suggests that goniomonad genetic diversity might equal that of the cryptophytes. Phylogenetic analysis of 10 Goniomonas sequences shows two very robust clades, one consisting only of 'G. truncata' and the other comprising G. pacifica-related sequences and a separate cluster of genotypes that probably represent G. amphinema. Thus, one clade comprises five freshwater strains, which have markedly longer genes, and the other clade comprises five marine strains. The divergence between all freshwater and all marine sequences is several times greater than that within one morphospecies. This deep genetic divergence implies that for several hundred million years, freshwater goniomonads have not been able to colonize marine habitats effectively, and vice versa. Our trees show that the 18S rRNA gene has evolved in freshwater strains faster than in the marine strains and robustly support the holophyly of all goniomonads and their sister relationship with cryptophytes.

Cosmopolitan microbes and their ‘cryptic’ species

“…The corresponding data on gene sequences data are, however, too limited to determine whether the marine and freshwater strains represent separate clusters in terms of rRNA gene sequences. Such clusters of marine and limnic isolates of goniomonad flagellates were, however, demonstrated by Von der Heyden et al (2004b). Similarly, B. J.…”

Molecular Comparisons of Freshwater and Marine Isolates of the Same Morphospecies of Heterotrophic Flagellates

“…Since this is apparently not the case, the observed pattern must be the result of different ecophysiological traits (13). The ecological differences between marine and freshwater habitats are therefore sufficient barriers for dispersal of at least some lineages of A. sigmoides, as previously reported for Goniomonas (37). The phylogeny of protistan morphospecies can therefore serve as an indicator of ecophysiological differentiation below the morphospecies level.…”

“…A study of strains of the flagellate Oxyrrhis marina showed that different salinity preferences and levels of salinity tolerance could be associated with different types of habitats (26). Von der Heyden et al (37) reported that there is clear divergence between marine and freshwater lineages of the flagellate Goniomonas.…”

Molecular characterisation of the small-eukaryote community in a tropical Great Lake (Lake Tanganyika, East Africa)

“…5 & 6), LT small-eukaryote assemblages appeared as a good example of the well-known barrier between microbial communities in freshwater and marine environments (e.g. Logares et al 2007, von der Heyden et al 2004). On the other hand, even if environmental clones from temperate freshwater systems appeared first, the average similarity was still rather low, which is indicative of an obvious undersampling of freshwater systems.…”

“…Amaral Zettler et al 2002, Lefranc et al 2005, Richards et al 2005, Lefèvre et al 2007, Chen et al 2008, despite the common divergence between freshwater and marine lineages within taxa (e.g. von der Heyden et al 2004, Logares et al 2007). In particular, small-eukaryote assemblages in tropical lakes have received no attention.…”