Dating Alphaproteobacteria evolution with eukaryotic fossils

Sishuo Wang,Haiwei Luo

doi:10.1038/s41467-021-23645-4

Abstract

Elucidating the timescale of the evolution of Alphaproteobacteria, one of the most prevalent microbial lineages in marine and terrestrial ecosystems, is key to testing hypotheses on their co-evolution with eukaryotic hosts and Earth’s systems, which, however, is largely limited by the scarcity of bacterial fossils. Here, we incorporate eukaryotic fossils to date the divergence times of Alphaproteobacteria, based on the mitochondrial endosymbiosis that mitochondria evolved from an alphaproteobacterial lineage. We estimate that Alphaproteobacteria arose ~1900 million years (Ma) ago, followed by rapid divergence of their major clades. We show that the origin of Rickettsiales, an order of obligate intracellular bacteria whose hosts are mostly animals, predates the emergence of animals for ~700 Ma but coincides with that of eukaryotes. This, together with reconstruction of ancestral hosts, strongly suggests that early Rickettsiales lineages had established previously underappreciated interactions with unicellular eukaryotes. Moreover, the mitochondria-based approach displays higher robustness to uncertainties in calibrations compared with the traditional strategy using cyanobacterial fossils. Further, our analyses imply the potential of dating the (bacterial) tree of life based on endosymbiosis events, and suggest that previous applications using divergence times of the modern hosts of symbiotic bacteria to date bacterial evolution might need to be revisited.

Highlights

Elucidating the timescale of the evolution of Alphaproteobacteria, one of the most prevalent microbial lineages in marine and terrestrial ecosystems, is key to testing hypotheses on their co-evolution with eukaryotic hosts and Earth’s systems, which, is largely limited by the scarcity of bacterial fossils
We develop a new strategy to date the divergence times of Alphaproteobacteria based on the mitochondrial endosymbiosis that the mitochondrion was derived from a bacterial lineage[19], whose phylogenetic position was later shown to be within[2,3,20] or closely related to[21] Alphaproteobacteria by modern phylogenetic analysis
We employed rigorous approaches to delineate phylogenetic artefacts caused by long-branch attraction and compositional heterogeneity, and obtained results consistent with recent studies where (i) Rickettsiales, Holosporales, and Pelagibacterales (SAR11) had independent origins[22], and (ii) mitochondria branched as a sister to Alphaproteobacteria[21] (Supplementary Fig. 1A)

Summary

Introduction

Elucidating the timescale of the evolution of Alphaproteobacteria, one of the most prevalent microbial lineages in marine and terrestrial ecosystems, is key to testing hypotheses on their co-evolution with eukaryotic hosts and Earth’s systems, which, is largely limited by the scarcity of bacterial fossils. If in an HGT event the recipient has fossil records while the donor does not, the temporal information recorded in the recipient can be transferred to date the evolution of the donor group (and vice versa), thereby bypassing the paucity of fossils in the donor lineage Inspired by this idea, we develop a new strategy to date the divergence times of Alphaproteobacteria based on the mitochondrial endosymbiosis that the mitochondrion was derived from a bacterial lineage[19], whose phylogenetic position was later shown to be within[2,3,20] or closely related to[21] Alphaproteobacteria by modern phylogenetic analysis. As mitochondria are characteristic of eukaryotes, here we take advantage of eukaryotic fossils to anchor the divergence time of Alphaproteobacteria in a tree integrating both alphaproteobacterial and mitochondrial lineages

Methods

Results

Conclusion