Multiple secondary origins of the anaerobic lifestyle in eukaryotes

Abstract

Classical ideas for early eukaryotic evolution often posited a period of anaerobic evolution producing a nucleated phagocytic cell to engulf the mitochondrial endosymbiont, whose presence allowed the host to colonize emerging aerobic environments. This idea was given credence by the existence of contemporary anaerobic eukaryotes that were thought to primitively lack mitochondria, thus providing examples of the type of host cell needed. However, the groups key to this hypothesis have now been shown to contain previously overlooked mitochondrial homologues called hydrogenosomes or mitosomes; organelles that share common ancestry with mitochondria but which do not carry out aerobic respiration. Mapping these data on the unfolding eukaryotic tree reveals that secondary adaptation to anaerobic habitats is a reoccurring theme among eukaryotes. The apparent ubiquity of mitochondrial homologues bears testament to the importance of the mitochondrial endosymbiosis, perhaps as a founding event, in eukaryotic evolution. Comparative study of different mitochondrial homologues is needed to determine their fundamental importance for contemporary eukaryotic cells.

Figure 1

Phylogenetic tree showing the evolutionary relationships between pyruvate:ferredoxin oxidoreductase (PFO) sequences from eukaryotes and eubacteria. Eukaryotes are shown in bold. The tree is a consensus tree from a Bayesian analysis of aligned protein sequences using custom software (available from p.foster@nhm.ac.uk). Aligned positions (715 sites) were recoded into the six Dayhoff groups: C, STPAG, NDEQ, HRK, MILV and FYW to reduce the effects of mutational saturation (Hrdy et al. 2004). Posterior probabilities for some groups are shown, with a value of 1.0 representing maximum support. The strongly supported groups have also been recovered in previously published analyses using different methods, including maximum-likelihood, and different support measures including bootstrapping (Horner et al. 1999; Rotte et al. 2001).

Figure 2

Phylogenetic tree showing the evolutionary relationships between [Fe]-hydrogenase sequences from eukaryotes and eubacteria. Eukaryotes are shown in bold. Details of the analysis on 196 aligned positions are given in the legend to figure 1. The strongly supported groups have also been recovered in previously published analyses using different methods, including maximum-likelihood, and different support measures including bootstrapping (Horner et al. 2000).