Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event

Abstract

Cyanobacteria are among the most diverse prokaryotic phyla, with morphotypes ranging from unicellular to multicellular filamentous forms, including those able to terminally (i.e., irreversibly) differentiate in form and function. It has been suggested that cyanobacteria raised oxygen levels in the atmosphere around 2.45-2.32 billion y ago during the Great Oxidation Event (GOE), hence dramatically changing life on the planet. However, little is known about the temporal evolution of cyanobacterial lineages, and possible interplay between the origin of multicellularity, diversification of cyanobacteria, and the rise of atmospheric oxygen. We estimated divergence times of extant cyanobacterial lineages under Bayesian relaxed clocks for a dataset of 16S rRNA sequences representing the entire known diversity of this phylum. We tested whether the evolution of multicellularity overlaps with the GOE, and whether multicellularity is associated with significant shifts in diversification rates in cyanobacteria. Our results indicate an origin of cyanobacteria before the rise of atmospheric oxygen. The evolution of multicellular forms coincides with the onset of the GOE and an increase in diversification rates. These results suggest that multicellularity could have played a key role in triggering cyanobacterial evolution around the GOE.

Fig. 1.

Time calibrated phylogeny of cyanobacteria displaying divergence time estimates. Bayesian consensus tree (analysis 7) based on 16S rRNA data with 95% highest posterior densities of the discussed node ages shown as green bars (analyses 1, 3, 5, and 7 overlapping). Morphological features of taxa are marked by colored boxes and listed in the inset. Full taxon names are displayed in Table S3. Branches with posterior probabilities >0.9 in all analyses are presented as thick lines. Gray circles mark points used for calibration of the tree. Details of the prior age estimates used for calibration are presented in Table 1. A significant increase in diversification rate (yellow triangle) [9.66-fold (average of all analyses)] can be detected at node 3 and a minor decrease (red triangle) at 33/34. The earlier shift close to node 3 coincides with the origin of multicellularity. Schematic drawings of cyanobacterial fossils are provided under the timeline, with the ones used for calibration of the tree marked in red. Our results indicate that multicellularity (green shade) originated before or at the beginning of the GOE.

Fig. 2.

Median age estimates under eight analytical scenarios. Median age estimates of clades (Table 1). The origin of cyanobacteria (node 1) and the evolution of multicellularity (node 3) are estimated before or at the beginning of the GOE. Relatively soon after the GOE, the stem lineages of the three major cyanobacterial clades originated, containing unicellular cyanobacteria (node 6), terminally differentiated taxa (node 31), and marine phycoplankton (node 43).

Fig. 3.

Prior and posterior probability distributions of ages for node 3. Marginal prior probability distributions of analyses using narrow (analysis 5) and wide (analysis 6) prior distributions were conservatively biased toward younger ages, strongly favoring an origin of multicellularity after the GOE. Even so, posterior probabilities point to an origin of multicellularity before or at the beginning of the GOE, indicating that this main result is based on a strong signal in the data rather than a bias from a-priori assumptions. Marginal prior probability distributions were estimated in analyses that only sampled from the prior.