Detection of Seven Major Evolutionary Lineages in Cyanobacteria Based on the 16S rRNA Gene Sequence Analysis with New Sequences of Five Marine Synechococcus Strains

Abstract

Although molecular phylogenetic studies of cyanobacteria on the basis of the 16S rRNA gene sequence have been reported, the topologies were unstable, especially in the inner branchings. Our analysis of 16S rRNA gene phylogeny by the maximum-likelihood and neighbor-joining methods combined with rate homogeneous and heterogeneous models revealed seven major evolutionary lineages of the cyanobacteria, including prochlorophycean organisms. These seven lineages are always stable on any combination of these methods and models, fundamentally corresponding to phylogenetic relationships based on other genes, e.g., psbA, rbcL, rnpB, rpoC, and tufA. Moreover, although known genotypic and phenotypic characters sometimes appear paralleled in independent lineages, many characters are not contradictory within each group. Therefore we propose seven evolutionary groups as a working hypothesis for successive taxonomic reconstruction. New 16S rRNA sequences of five unicellular cyanobacterial strains, PCC 7001, PCC 7003, PCC 73109, PCC 7117, and PCC 7335 of Synechococcus sp., were determined in this study. Although all these strains have been assigned to "marine clusters B and C," they were separated into three lineages. This suggests that the organisms classified in the genus Synechococcus evolved diversely and should be reclassified in several independent taxonomic units. Moreover, Synechococcus strains and filamentous cyanobacteria make a monophyletic group supported by a comparatively high statistical confidence value (80 to 100%) in each of the two independent lineages; therefore, these monophylies probably reflect the convergent evolution of a multicellular organization.

Species concepts and speciation factors in cyanobacteria, with connection to the problems of diversity and classification

“…cell morphology) may at times be phylogenetically uninformative when compared to phylogenies generated by 16S rRNA gene data, which is the currently accepted ''Gold-standard'' in bacterial systematics (e.g. Honda et al 1999;Robertson et al 2001;Kim et al 2014).…”

“…Synechococcus sensu lato is a group of cyanobacteria with cosmopolitan distribution inhabiting almost all environments (Komárek and Anagnostidis 1998), including thermal and aerophytic habitats (Honda et al 1999;Robertson et al 2001). Although some cyanobacteria, such as Synechococcus sensu lato, lack phenotypic variability, great ecological and genetic diversity suggest that polyphyletic complexes of cryptic taxa might exist (Honda et al 1999;Robertson et al 2001;Dvořák et al 2014a, b).…”

“…Although some cyanobacteria, such as Synechococcus sensu lato, lack phenotypic variability, great ecological and genetic diversity suggest that polyphyletic complexes of cryptic taxa might exist (Honda et al 1999;Robertson et al 2001;Dvořák et al 2014a, b). Many traditional cyanobacterial genera (Geitler 1932) are polyphyletic (Komárek 2010;Engene et al 2011;Hašler et al 2012;Engene et al 2013;Dvořák et al 2014a, b;Hašler et al 2014a) and need extensive revisions, which will be very difficult particularly in the case of Synehococcus sensu lato due to extreme polyphyly within this genus.…”

“…Such convergent events might be explained by HGT within the environment and therefore environmental pressures (Litvaitis 2002). It is also likely that it represents a frequent trend in cyanobacterial evolution, since other morphological traits, such as multicellularity, have evolved repeatedly (Honda et al 1999;Robertson et al 2001;Schirrmeister et al 2013;Dvořák et al 2014a, b). Dvořák et al (2014b, Fig.…”

The Yfr2 ncRNA family, a group of abundant RNA molecules widely conserved in cyanobacteria

“…Interestingly, the fourth copy can be found 3' to this histidine kinase gene in the Ava_3819-purH intergenic spacer. The closely related strain Nostoc punctiforme has one Yfr2 homolog less than A. variabilis and Anabaena PCC7120 and lacks the histidine kinase gene in In phylogenetic analyses Gloeobacter violaceus frequently appears as an early branching or even the most ancestral cyanobacterium, 11,12 which is consistent with its cell biology (the only cyanobacterium lacking thylakoids). Since we did not find a Yfr2 gene copy in this organism, it is possible that this ncRNA family has evolved only later within the cyanobacterial phylum.…”