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Dating Alphaproteobacteria Evolution with Eukaryotic Fossils ✉ Sishuo Wang 1 & Haiwei Luo 1,2,3

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Dating Alphaproteobacteria Evolution with Eukaryotic Fossils ✉ Sishuo Wang 1 & Haiwei Luo 1,2,3 ARTICLE https://doi.org/10.1038/s41467-021-23645-4 OPEN Dating Alphaproteobacteria evolution with eukaryotic fossils ✉ Sishuo Wang 1 & Haiwei Luo 1,2,3 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 1234567890():,; 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 uni- cellular 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. 1 Simon F. S. Li Marine Science Laboratory, School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, SAR, Hong Kong. 2 Shenzhen Research Institute, The Chinese University of Hong Kong, Shenzhen, China. 3 Hong Kong Branch of Southern Marine ✉ Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, SAR, Hong Kong. email: [email protected] NATURE COMMUNICATIONS | (2021) 12:3324 | https://doi.org/10.1038/s41467-021-23645-4 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-021-23645-4 he Alphaproteobacteria is one of the largest groups within variations among branches. The first data set, which we referred bacteria1 and of great evolutionary significance for holding to as the mito-encoded data set, was based on the aforementioned T 2,3 the origin of the mitochondrion . The Alphaproteo- 24 conserved genes encoded by mitochondrial genomes (Sup- bacteria has extensively diversified since its ancient origin, and plementary Data 1), and the mitochondrial lineages mainly comprise some of the most environmentally abundant and comprising species of green plants, red algae, and jakobids, whose metabolically diverse organisms on Earth1,4,5. Alphaproteo- mitochondrial genomes are both gene-rich and relatively slowly bacteria represent 40–50% of bacterioplankton cells in sunlit evolving21,24. Four high-confidence fossils from land plants and oceans and 20–30% in dark oceans6,7, and account for ~30% of red algae were used as the calibration points (Supplementary the dominant phylotypes of bacteria in global soils8. Besides, the Note 2.1; Supplementary Fig. 2A). The second data set, referred to intimate association between some alphaproteobacterial lineages as the nuclear-encoded data set, was based on 22 mitochondria- and eukaryotes is of central importance for agricultural (e.g., derived genes that had been transferred to the nuclear genome rhizobia) and medical (e.g., rickettsia) applications. This makes identified by Wang and Wu3 (Supplementary Data 1). This data Alphaproteobacteria a promising system to study the timing of set not only circumvented the problem that in many eukaryotes bacterial evolution and their correlation with geological, ecolo- genes encoded by mitochondrial genomes are few (e.g., apicom- gical, and evolutionary events5,9,10. However, the traditional way plexans and dinoflagellates) or fast-evolving (e.g., animals and of divergence time estimation has several limits when applied to fungi)25, but integrated six additional eukaryotic fossils (Supple- Alphaproteobacteria and other prokaryotes. First, fossil records of mentary Fig. 2A; Supplementary Note 2.1), allowing directly bacteria are extremely scarce and controversial in terms of their comparing the divergence time between animal symbionts and estimated dates11. Second, the most widely used prokaryotic their hosts on the same tree. fossils are from cyanobacteria, but the long evolutionary distance We selected a best-practiced scheme based on systematic between cyanobacteria and other bacteria causes large uncer- comparisons of different combinations of parameters of tainties in dating12. Last, some studies13,14 assumed a strict MCMCTree for the mito- and nuclear-encoded data sets (see relationship of bacteria-host evolution and calibrated the evolu- Methods and Supplementary Note 1.2). Similar divergence times tion of symbiotic bacteria based on the divergence time of their were recovered for most nodes between the two data sets, modern hosts (mostly animals and plants). However, this pre- although the mito-encoded data set estimated older ages for deep cludes the possibility of host switching, which could occur fre- nodes (Fig. 1). As shown in the infinite-sites plots (up- and quently during evolutionary processes spanning millions of bottom-left panels in Fig. 1), the posterior mean ages versus 95% years9. Owing to these challenges, the origin time of Alphapro- HPD (highest posterior density) widths approached a straight teobacteria estimated by previous studies varies from <600 mil- line, suggesting that the uncertainty in time estimate was lion years (Ma) to >2000 Ma5,14–16, making any narratives based predominantly caused by the uncertainty associated with fossil on its evolutionary timing contentious. calibrations26. The estimated ages in the nuclear-encoded data set Recently, horizontal gene transfer (HGT) has been suggested to exhibited smaller 95% HPD intervals, hence smaller uncertainties, have great potential in dating the evolution of bacteria17,18.In likely owing to their more calibration information compared with brief, if in an HGT event the recipient has fossil records while the the mito-encoded data set. donor does not, the temporal information recorded in the reci- Most alphaproteobacterial orders diverged 1500–1000 Mya, pient can be transferred to date the evolution of the donor group and Rickettsiales and Pelagibacterales appeared to be the oldest (and vice versa), thereby bypassing the paucity of fossils in the and youngest alphaproteobacterial orders, respectively, based on donor lineage. Inspired by this idea, we develop a new strategy to the taxa sampled here (Fig. 1). The origin time of Rickettsiales,an date the divergence times of Alphaproteobacteria based on the obligate endosymbiont lineage whose hosts cover diverse mitochondrial endosymbiosis that the mitochondrion was eukaryotes but mostly animals27, was estimated to be 1741 Ma derived from a bacterial lineage19, whose phylogenetic position (95% HPD 1975–1514 Ma) and 1607 Ma (95% HPD 1767–1467 was later shown to be within2,3,20 or closely related to21 Alpha- Ma) using the mito- and nuclear-encoded data sets, respectively proteobacteria by modern phylogenetic analysis. As mitochondria (Fig. 1). One merit of our mitochondria-based method is that are characteristic of eukaryotes, here we take advantage of divergence times of the eukaryotic hosts and of the host- eukaryotic fossils to anchor the divergence time of Alphaproteo- associated bacteria can be simultaneously estimated. As shown in bacteria in a tree integrating both alphaproteobacterial and Fig. 1, we dated the origin of animals (Metazoa) to be 814 Ma mitochondrial lineages. (95% HPD 850–769 Ma), consistent with previous dating analyses28–30, but not others31. We also estimated that mitochon- drial lineages diverged from Alphaproteobacteria ~1900 Mya Results (million years ago) and that the last common ancestor (LCA) The evolutionary timescale of Alphaproteobacteria estimated of mitochondria occurred ~1550 Mya (Fig. 1). Thus, the origin of by a mitochondria-based strategy.Wefirst reconstructed a Rickettsiales likely predated the evolutionary emergence of phylogenomic tree of 80 carefully selected Alphaproteobacteria animals for ~700 Ma but coincided with the mitochondrial and mitochondrial genomes using 24 conserved genes based on endosymbiosis process and the occurrence of the LCA of prior phylogenomics studies21,22 (see Methods and Supplemen- eukaryotes, according to our (Fig. 1) and others’ estimates28,29,32, tary Note 1.1). We employed rigorous approaches to delineate and fossil records (reviewed in Butterfield33). This agrees with phylogenetic artefacts caused by long-branch attraction and recent findings of an increasingly broad range of protistan hosts compositional heterogeneity (see Methods), and obtained results of Rickettsiales (reviewed in Castelli et al[.34), and suggests that consistent with recent studies where (i) Rickettsiales, Holosporales, host switches to animals from protists occurred later in the and Pelagibacterales (SAR11) had independent origins22, and (ii) evolution of Rickettsiales. The origin time of Holosporales, mitochondria branched as a sister to Alphaproteobacteria21 another important endosymbiotic lineage in Alphaproteobacteria (Supplementary Fig. 1A). We also
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