Cyanobacterial symbionts diverged in the late Cretaceous towards lineage-specific nitrogen fixation factories in single-celled phytoplankton

Abstract

The unicellular cyanobacterium UCYN-A, one of the major contributors to nitrogen fixation in the open ocean, lives in symbiosis with single-celled phytoplankton. UCYN-A includes several closely related lineages whose partner fidelity, genome-wide expression and time of evolutionary divergence remain to be resolved. Here we detect and distinguish UCYN-A1 and UCYN-A2 lineages in symbiosis with two distinct prymnesiophyte partners in the South Atlantic Ocean. Both symbiotic systems are lineage specific and differ in the number of UCYN-A cells involved. Our analyses infer a streamlined genome expression towards nitrogen fixation in both UCYN-A lineages. Comparative genomics reveal a strong purifying selection in UCYN-A1 and UCYN-A2 with a diversification process ∼91 Myr ago, in the late Cretaceous, after the low-nutrient regime period occurred during the Jurassic. These findings suggest that UCYN-A diversified in a co-evolutionary process, wherein their prymnesiophyte partners acted as a barrier driving an allopatric speciation of extant UCYN-A lineages.

On the origin of oxygenic photosynthesis and Cyanobacteria

“…For instance, the closest relatives (i.e. Molecular clock studies of symbiotic associations have also shown that age estimates of the symbiont, UCYN-A, overlap with fossil ages of its host, Braarudosphaera bigelowii, at c. 92 Ma (Cornejo-Castillo et al, 2016). In more recent time scales, the age estimation of marine planktonic groups is consistent with geochemical evidence supporting the timing of the ocean oxygenation at c. 800-600 Ma (S anchez- .…”

Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment

“…Because of the physical, direct interaction between bacteria and phytoplankton cells, the attachment strategy could provide both components with an ecological advantage compared with their free-living counterparts (Rooney-Varga et al, 2005;Grossart and Simon, 2007a;Grossart et al, 2007b). Indeed, it has been recently observed that symbiotic relationships between cyanobacteria and microalgae through attachment are key strategies for C and N exchange between them (Thompson et al, 2012;Cornejo-Castillo et al, 2016).…”

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

“…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.…”

“…The UCYN-A based symbioses (both DNA and RNA based samples) have been reported in the TARA project and from a few select stations Cornejo-Castillo et al, 2016), while the DDAs remain un-reported. Using several genetic markers derived from the DDA symbionts (16S rRNA, nifH) and hosts (rbcL, 18S rRNA), we performed blast searches in the KEGG MGENES (www.genome.jp/mgenes/) and in the IMNGS database (https:// www.imngs.org/), with a 95% identity cut off.…”

“…A closer look at the two symbioses reveals that the housing of the symbionts are quite similar. For example, in prymnesiophyte hosts, UCYN-A have been described as internal symbionts by TEM observations of the host cytoplasm, loosely attached or in a free-floating compartment (symbiosome) (Hagino et al, 2013;Cornejo-Castillo et al, 2016). The symbionts of the DDAs vary from externally attached to a quasi-internal location residing between the host frustule and plasma membrane (Villareal, 1992).…”