A Major Clade of Prokaryotes with Ancient Adaptations to Life on Land

Abstract

Evolutionary trees of prokaryotes usually define the known classes and phyla but less often agree on the relationships among those groups. This has been attributed to the effects of horizontal gene transfer, biases in sequence change, and large evolutionary distances. Furthermore, higher level clades of prokaryote phyla rarely are supported by information from ecology and cell biology. Nonetheless, common patterns are beginning to emerge as larger numbers of species are analyzed with sophisticated methods. Here, we show how combined evidence from phylogenetic, cytological, and environmental data support the existence of an evolutionary group that appears to have had a common ancestor on land early in Earth's history and includes two-thirds of known prokaryote species. Members of this terrestrial clade (Terrabacteria), which includes Cyanobacteria, the gram-positive phyla (Actinobacteria and Firmicutes), and two phyla with cell walls that differ structurally from typical gram-positive and gram-negative phyla (Chloroflexi and Deinococcus-Thermus), possess important adaptations such as resistance to environmental hazards (e.g., desiccation, ultraviolet radiation, and high salinity) and oxygenic photosynthesis. Moreover, the unique properties of the cell wall in gram-positive taxa, which likely evolved in response to terrestrial conditions, have contributed toward pathogenicity in many species. These results now leave open the possibility that terrestrial adaptations may have played a larger role in prokaryote evolution than currently understood.

Diversification rates and species richness across the Tree of Life

“…We also assembled the trees into an overall phylogeny spanning the Tree of Life, for comparative analyses (figure 1). For the backbone of the tree, we used a time-calibrated phylogeny of Eubacteria [21] and an estimate for the age of origin of Archaea [22]. To this backbone, we then added a time-calibrated phylogeny of major eukaryote clades [15].…”

Insights into the phylogeny and coding potential of microbial dark matter

“…2). Candidate phylum OP11, as originally proposed 26 , has not been resolved consistently as a monophyletic group leading to the proposal for subdivision into multiple phyla, including OP11 (former subdivisions 1 to 3 only), OD1 (former OP11 subdivision 5) and SR1 (ref. 31).…”

“…The Terrabacteria, proposed to comprise the 'terrestrial' bacterial phyla Actinobacteria, Cyanobacteria, Thermi (Deinococcus-Thermus), Chloroflexi and Firmicutes 26 , was resolved in our analysis with the additional membership of Armatimonadetes (former candidate phylum OP10) 27 ( Fig. 2).…”

“…2). Perhaps more compelling than the assertion of ancient adaptations to life on land unifying the Terrabacteria 26 are commonalities in cell envelope architecture. This superphylum comprises monoderm (single membrane) and atypical monoderm lineages 28 .…”

Stone-dwelling actinobacteria Blastococcus saxobsidens, Modestobacter marinus and Geodermatophilus obscurus proteogenomes

“…They also have the ability to resist adverse environmental conditions such as ultraviolet light, ionizing radiation, desiccation and heavy metals (Rainey et al, 2005;Gtari et al, 2012;Montero-Calasanz et al, 2014, 2015. This resistance to environmental hazards represents a trait of Terrabacteria, a well-supported phylogenetic group composed of Actinobacteria and four other major lineages of eubacteria (Firmicutes, Cyanobacteria, Chloroflexi and Deinococcus-Thermus) that colonized land 3.05-2.78 Ga (Tunnacliffe and Lapinski, 2003;Battistuzzi et al, 2004;Battistuzzi and Hedges, 2009).…”