Comparative genomics reveals surprising divergence of two closely related strains of uncultivated UCYN-A cyanobacteria

Abstract

Marine planktonic cyanobacteria capable of fixing molecular nitrogen (termed 'diazotrophs') are key in biogeochemical cycling, and the nitrogen fixed is one of the major external sources of nitrogen to the open ocean. Candidatus Atelocyanobacterium thalassa (UCYN-A) is a diazotrophic cyanobacterium known for its widespread geographic distribution in tropical and subtropical oligotrophic oceans, unusually reduced genome and symbiosis with a single-celled prymnesiophyte alga. Recently a novel strain of this organism was also detected in coastal waters sampled from the Scripps Institute of Oceanography pier. We analyzed the metagenome of this UCYN-A2 population by concentrating cells by flow cytometry. Phylogenomic analysis provided strong bootstrap support for the monophyly of UCYN-A (here called UCYN-A1) and UCYN-A2 within the marine Crocosphaera sp. and Cyanothece sp. clade. UCYN-A2 shares 1159 of the 1200 UCYN-A1 protein-coding genes (96.6%) with high synteny, yet the average amino-acid sequence identity between these orthologs is only 86%. UCYN-A2 lacks the same major pathways and proteins that are absent in UCYN-A1, suggesting that both strains can be grouped at the same functional and ecological level. Our results suggest that UCYN-A1 and UCYN-A2 had a common ancestor and diverged after genome reduction. These two variants may reflect adaptation of the host to different niches, which could be coastal and open ocean habitats.

Global distribution and vertical patterns of a prymnesiophyte–cyanobacteria obligate symbiosis

“…This is in agreement with a greater contribution of B. bigelowii reads in the 0.8-5 μm size fraction (as compared with the 5-20 μm fraction) in the Tara-Oceans metabarcoding data analyzed here, as well as of UCYN-A2 reads in the same smaller size fraction in metagenomic samples of the South Atlantic (Cornejo-Castillo et al, submitted). The hypothesis about the obligatory dependence of UCYN-A with its host (Tripp et al, 2010;Thompson et al, 2012;Bombar et al, 2014) has been recently reinforced with the strong coupling observed in the transfer of carbon and nitrogen metabolites between partner cells (Krupke et al, 2014b). On the other hand, the possibility of a freeliving population of the host could not be evaluated as the FISH probe used in previous studies (Krupke et al, 2014a) targeted the whole prymnesiophyte assemblage and not the specific host phylotypes.…”

Cyanobacterial evolution during the Precambrian

“…Studies have questioned the bifurcating history of the tree of life, due to genetic exchange via lateral gene transfer (LGT; Ochman et al 2000;Kunin et al 2005). Yet, even though LGT can occur, as shown for example at threonyl tRNA synthease (Zhaxybayeva et al 2006), ribosomal genes seem to be rather conserved (Schirrmeister et al 2012) and large-scale multi-gene phylogenetic analyses have improved our understanding of cyanobacteria and reconstructed the phylum's history with increased statistical support for deep-branching (Shih et al 2013;Bombar et al 2014;Sanchez-Baracaldo et al 2014;Schirrmeister et al 2015).…”

A Short Comparison of Two Marine Planktonic Diazotrophic Symbioses Highlights an Un-quantified Disparity

“…As reported earlier, the genomes of UCYN-A1 and UCYN-A2 are similar in size, content, and streamlining (Bombar et al, 2014); while the DDA symbiont draft genomes differ largely (Figure 1, Table 1), and content appears influenced by the symbiont location (Hilton et al, 2013).…”

“…The prymnesiophyte-UCYN-A symbioses are small in comparison; both hosts and symbionts are <10 µm. In fact a closer examination at the size fractionation experiments reported in Tripp et al (2010) (Figure 4, Tripp et al, 2010), demonstrates Villareal, 1992;Foster and Zehr, 2006;Foster and O'Mullan, 2008;Zehr et al, 2008;Tripp et al, 2010;Thompson et al, 2012Thompson et al, , 2014Hagino et al, 2013;Hilton et al, 2013;Krupke et al, 2013;Bombar et al, 2014;Hilton, 2014;Cabello et al, 2016;Cornejo-Castillo et al, 2016;Martínez-Pérez et al, 2016. √ up to 13 species are reported for Rhizosolenia-R. intracellularis symbioses hence we report the two most common.…”

“…There is an additional draft Richelia genome (RintRC01) now available (Hilton, 2014). Two UCYN-A genomes are available, one is closed, and a second is open (Zehr et al, 2008;Tripp et al, 2010;Bombar et al, 2014). We excluded the DDA symbiont RintHM01 as it was reduced and lacked genes expected for a full genome (Hilton, 2014).…”