A New Analysis of Archaea–Bacteria Domain Separation: Variable Phylogenetic Distance and the Tempo of Early Evolution

Abstract

Comparative genomics and molecular phylogenetics are foundational for understanding biological evolution. Although many studies have been made with the aim of understanding the genomic contents of early life, uncertainty remains. A study by Weiss et al. (Weiss MC, Sousa FL, Mrnjavac N, Neukirchen S, Roettger M, Nelson-Sathi S, Martin WF. 2016. The physiology and habitat of the last universal common ancestor. Nat Microbiol. 1(9):16116.) identified a number of protein families in the last universal common ancestor of archaea and bacteria (LUCA) which were not found in previous works. Here, we report new research that suggests the clustering approaches used in this previous study undersampled protein families, resulting in incomplete phylogenetic trees which do not reflect protein family evolution. Phylogenetic analysis of protein families which include more sequence homologs rejects a simple LUCA hypothesis based on phylogenetic separation of the bacterial and archaeal domains for a majority of the previously identified LUCA proteins (∼82%). To supplement limitations of phylogenetic inference derived from incompletely populated orthologous groups and to test the hypothesis of a period of rapid evolution preceding the separation of the domains, we compared phylogenetic distances both within and between domains, for thousands of orthologous groups. We find a substantial diversity of interdomain versus intradomain branch lengths, even among protein families which exhibit a single domain separating branch and are thought to be associated with the LUCA. Additionally, phylogenetic trees with long interdomain branches relative to intradomain branches are enriched in information categories of protein families in comparison to those associated with metabolic functions. These results provide a new view of protein family evolution and temper claims about the phenotype and habitat of the LUCA.

Radiation of nitrogen‐metabolizing enzymes across the tree of life tracks environmental transitions in Earth history

“…Similarly, phylogenetic reconstructions showing that Mo‐nitrogenases arose before V‐ and Fe‐nitrogenases are consistent with this conclusion (Garcia et al., 2020). It has been argued that nitrogenase was present in LUCA (Weiss et al., 2016), though that has been disputed (Berkemer & McGlynn, 2020; Boyd, et al., 2011; Mus et al., 2019) and our results do not resolve this issue. However, the identification of horizontal gene transfer events for nitrogenase subunits during the Archean (Figure 3) suggest that this metabolism may have been abundant and beneficial enough during this time period to have been successfully transferred and retained in microbial genomes.…”

On the evolution of chaperones and co-chaperones and the expansion of proteomes across the Tree of Life

“…The protein tree of HSP20-an anti-aggregation 'holding' chaperone depicted a clear single split of bacterial and archaeal domains at the root, albeit with weak bootstrap support, and inter-kingdom branch lengths were shorter than intra-kingdom branch-lengths (Table S1). Similar uncertainties were noted for the majority of protein families formerly assigned to LUCA (Berkemer and McGlynn, 2020). Previous studies assigned HSP20 to LUCA (Sousa et al, 2016;Weiss et al, 2016), which, despite the above uncertainties, we concur ( Figure 3A).…”

“…Dating emergence to LUCA is particularly challenging. We followed the recommendations of Berkemer and McGlynn (Berkemer and McGlynn, 2020) and demanded that for a chaperone family to be assigned to LUCA, there must be a single split between bacterial and archaeal sequences at the root of the protein tree, with strong bootstrap support for this split, and that inter-kingdom branches would be longer than the intra-kingdom branches. These criteria assigned the emergence of only one corechaperone, HSP60-a cage-like ATP-fueled unfoldase (Finka et al, 2016;Saibil, 2013), to LUCA ( Figure 3A, Table S1).…”

Radiation of nitrogen-metabolizing enzymes across the tree of life tracks environmental transitions in Earth history

“…Similarly, phylogenetic reconstructions showing that Mo-nitrogenases arose before V-and Fe-nitrogenases are consistent with this conclusion (Garcia et al, 2020). It has been argued that nitrogenase was present in LUCA (Weiss et al, 2016), though that has been disputed (Boyd et al, 2011a;Mus et al, 2019;Berkemer & McGlynn, 2020) and our results do not resolve this issue. However, the identification of horizontal gene transfer events for nitrogenase subunits during the Archean (Figure 3) suggest that this metabolism may have been abundant and beneficial enough during this time period to have been successfully transferred and retained in microbial genomes.…”