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Abstract
The phylum Cyanobacteria includes free-living bacteria and plastids, the descendants of cyanobacteria that were engulfed by the ancestral lineage of the major photosynthetic eukaryotic group Archaeplastida. Endosymbiotic events that followed this primary endosymbiosis spread plastids across diverse eukaryotic groups. The remnants of the ancestral cyanobacterial genome present in all modern plastids, enable the placement of plastids within Cyanobacteria using sequence-based phylogenetic analyses. To date, such phylogenetic studies have produced conflicting results and two competing hypotheses: (1) plastids diverge relatively recently in cyanobacterial evolution and are most closely related to nitrogen-fixing cyanobacteria, or (2) plastids diverge early in the evolutionary history of cyanobacteria, before the divergence of most cyanobacterial lineages. Here, we use phylogenetic analysis of ribosomal proteins from an expanded data set of cyanobacterial and representative plastid genomes to infer a deep placement for the divergence of the plastid ancestor lineage. We recover plastids as sister to Gloeomargarita and show that the group diverges from other cyanobacterial groups before Pseudanabaena, a previously unreported placement. The tree topologies and phylogenetic distances in our study have implications for future molecular clock studies that aim to model accurate divergence times, especially with respect to groups containing fossil calibrations. The newly sequenced cyanobacterial groups included here will also enable the use of novel cyanobacterial microfossil calibrations.
Highlights
Two major groups of organisms produce oxygen by oxygenic photosynthesis: Cyanobacteria, the bacterial group in which this metabolism first evolved, and photosynthetic eukaryotes
These results are especially relevant to molecular clock studies that use cyanobacterial/plastid phylogenetic trees calibrated by fossil evidence, as accurate tree topologies are important for estimation of divergence times
The placement of plastids within a cyanobacterial phylogeny is key to understanding the evolutionary timing and relationship of these groups, but this placement remains in question
Summary
Two major groups of organisms produce oxygen by oxygenic photosynthesis: Cyanobacteria, the bacterial group in which this metabolism first evolved, and photosynthetic eukaryotes. A more recent analysis included a newly sequenced cyanobacterium (Gloeomargarita lithophora) and used a concatenation of 97 proteins chosen from plastid genomes to suggest a deep placement of plastids with G. lithophora as a sister group to their cyanobacterial ancestor (Ponce-Toledo et al, 2017) This result was further supported by phylogenies of concatenated 16S and 23S rRNA datasets, Bayesian consensus trees generated from these datasets did not resolve the deep relationship between Pseudanabaena, G. lithophora+plastids, and other more derived clades of cyanobacteria. These processes decrease the amount of phylogenetic information available for evolutionary inference and increase the chance of tree reconstruction artifacts such as long branch attraction Such factors have been noted in debates regarding the placement of the alphaproteobacterial ancestor lineage of mitochondria (Fitzpatrick et al, 2006; Ferla et al, 2013; Wang and Wu, 2015; Martijn et al, 2018), and may impact the nucleotide or amino acid sequences used in any given phylogenetics study to varying degrees. These results are especially relevant to molecular clock studies that use cyanobacterial/plastid phylogenetic trees calibrated by fossil evidence, as accurate tree topologies are important for estimation of divergence times
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