Distribution of a consortium between unicellular algae and the N₂ fixing cyanobacterium UCYN‐A in the North Atlantic Ocean

Abstract

Summary The globally abundant, uncultured unicellular cyanobacterium UCYN‐A was recently discovered living in association with a eukaryotic cell closely related to a prymnesiophyte. Here, we established a double CAtalysed Reporter Deposition‐Fluorescence In Situ Hybridization (CARD‐FISH) approach to identify both partners and provided quantitative information on their distribution and abundance across distinct water masses along a transect in the North Atlantic Ocean. The N2 fixation activity coincided with the detection of UCYN‐A cells and was only observed in oligotrophic (< 0.067 N boldO bold3 − μM and < 0.04 P boldO bold4 3 − μM) and warm (> 18°C) surface waters. Parallel 16S ribosomal RNA gene analyses among unicellular diazotrophs indicated that only UCYN‐A cells were present. UCYN‐A cells were associated with an algal partner or non‐associated using the double CARD‐FISH approach. We demonstrated that UCYN‐A cells living in association with Haptophyta were the dominant form (87.0 ± 6.1%), whereas non‐associated UCYN‐A cells represented only a minor fraction (5.2 ± 3.9%). Interestingly, UCYN‐A cells were also detected living in association with unknown single‐celled eukaryotes in small amounts (7.8 ± 5.2%), presumably Alveolata. The proposed ecological niche of UCYN‐A as an oligotrophic, mesophilic and obligate symbiotic nitrogen‐fixing microorganism is evident for the North Atlantic Ocean.

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

“…This supports previous observations from the North Pacific (Thompson et al, 2012) and the North Atlantic (Krupke et al, 2014a). …”

“…Characterization of the partnership Microscopic observations revealed a population size spectra and phenotype consistent with previous reports, with small prymnesiophyte host cells of 2-3 μm typically with one cyanobacterial UCYN-A1 symbiont (Thompson et al, 2012;Krupke et al, 2014a). On the other hand, the cell size of the UCYN-A2 host in open ocean samples was 4-5 μm, clearly smaller than that described in coastal sites, about 7-10 μm (Hagino et al, 2013;Thompson et al, 2014).…”

“…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. Our use of a specific probe for the UCYN-A1 host allowed us to validate that this association was also obligatory for the host as (i) we never observed a free-living population of targeted prymnesiophytes in the absence of UCYN-A and (ii) counts of free partner cells, when detected, were correlated, suggesting a disruption of the association owing to sample manipulation (Thompson et al, 2012;Krupke et al, 2013).…”

“…The double CARD-FISH assay was already used for the same symbiosis (Krupke et al, 2014a) and followed the Multi-color CARD-FISH protocol (Pernthaler et al, 2004). Filters were embedded in 0.1% low gelling point agarose to minimize cell loss and treated with lysozyme (37°C, 1 h) and acromopeptidase (37°C, 0.5 h) to permeabilize cell covers.…”

High levels of heterogeneity in diazotroph diversity and activity within a putative hotspot for marine nitrogen fixation

“…This implies a potential role of phosphate limitation in the shift in diazotroph community composition. UCYN-A1 and γ-24774A11 both appear to be broadly distributed throughout low-nutrient marine waters (Thompson et al, 2014;Langlois et al, 2015), and it has been hypothesised that these taxa thrive in oligotrophic conditions (Church et al, 2008;Krupke et al, 2014). In line with our findings in the ATS and Coral Sea, Moisander et al (2014) recently demonstrated that γ-24774A11 was significantly negatively correlated to soluble reactive phosphorous in the western South Pacific.…”