Evolution of Patchily Distributed Proteins Shared between Eukaryotes and Prokaryotes: Dictyostelium as a Case Study

Abstract

Protein families are often patchily distributed in the tree of life; they are present in distantly related organisms, but absent in more closely related lineages. This could either be the result of lateral gene transfer between ancestors of organisms that encode them, or losses in the lineages that lack them. Here a novel approach is developed to study the evolution of patchily distributed proteins shared between prokaryotes and eukaryotes. Proteins encoded in the genome of cellular slime mold Dictyostelium discoideum and a restricted number of other lineages, including at least one prokaryote, were identified. Analyses of the phylogenetic distribution of 49 such patchily distributed protein families showed conflicts with organismal phylogenies; 25 are shared with the distantly related amoeboflagellate Naegleria (Excavata), whereas only two are present in the more closely related Entamoeba. Most protein families show unexpected topologies in phylogenetic analyses; eukaryotes are polyphyletic in 85% of the trees. These observations suggest that gene transfers have been an important mechanism for the distribution of patchily distributed proteins across all domains of life. Further studies of this exchangeable gene fraction are needed for a better understanding of the origin and evolution of eukaryotic genes and the diversification process of eukaryotes.

Gene Transfers Shaped the Evolution of De Novo NAD + Biosynthesis in Eukaryotes

“…The sequences next to this eukaryotic branch are from Kangiella koreensis and Kangiella aquimarina , marine bacteria from the family of Alcanivoracaceae, with several species in the North Atlantic. The co-occurrence of homologous proteins in distantly related organisms within the same environments has been observed before in studies of horizontal gene transfer both in prokaryotes (Beiko et al 2005) and in eukaryotes (Andersson 2011). …”

“…Earlier phylogenetic analyses of kynurenine-3-monooxygenases also place the sequence from Dictyostelium discoideum (Amoebozoa) in one branch with bacterial sequences (Lima et al 2009), in good agreement with our results. Phylogenomic analyses for the amoebozoans D. discoideum (Andersson 2011; Eichinger et al 2005) and Entamoeba histolytica (Loftus et al 2005) identified several instances of horizontal gene transfer from bacterial genomes, and it has been suggested that the phagotrophic life style of amoebozoa promoted DNA uptake (Doolittle 1998). Interestingly, none of the three phylogenomic studies with amoebozoa seem to have identified kynurenine-3-monooxygenase as a candidate for horizontal gene transfer.…”

The scale and evolutionary significance of horizontal gene transfer in the choanoflagellate Monosiga brevicollis

“…Theoretically, phagotrophic protists could acquire a large number of foreign genes from diverse food sources over time, and their diet may be reflected in the sources (or donors) of acquired genes. The proportion of acquired genes in Monosiga genome (4.4%) is considerably higher than reported in many protozoan eukaryotes [8, 9, 40, 43, 44], but is in line with those reported in some other free-living microbial eukaryotes such as the red alga Galdieria sulphuraria [45] and bdelloid rotifers [46]. The potential donors for these acquired genes include diverse microscopic algal lineages such as green algae ( Micromonas and Ostreococcus ), diatoms ( Thalassiosira and Phaeodactylum ), haptophytes ( Emiliania and Isochrysis ), pelagophytes ( Aureococcus ), as well as numerous bacterial taxa, all of which are abundant and coexist in the same marine habitat with M. brevicollis .…”

“…It has been suggested that individual prokaryotic organisms sample genes from a large global gene pool or pan-genome in response to shift in niches and resources [66, 67]. In eukaryotes, although acquired genes have been reported in many studies [7–9, 16, 44, 51, 68, 69], the overall scale of HGT in eukaryotes remains elusive. Because the evolutionary impact of HGT is largely correlated to the number of acquired genes, such a scale is critical for understanding genome evolution and speciation of recipient organisms.…”

Complex Patterns of Gene Fission in the Eukaryotic Folate Biosynthesis Pathway

“…This suggests a different or deeper ancestry of myosin II. Alternatively, this distribution pattern may be the result of HGT (Berney C, personal communication) with additional examples of HGT-derived genes shared by Heterolobosea and Amoebozoa (Andersson 2011; Herman et al 2013) supporting the idea that HGT between these groups has played a role. However, an amended version of the “bikont” and “unikont” bifurcation recently gained some direct support using a rooted multigene phylogenetic analysis of genes derived through the mitochondrial endosymbiosis (Derelle and Lang 2012), but also see He et al (2014) for an alternative tree topology derived from a similar analytical approach.…”