Genetic diversity of the unicellular nitrogen‐fixing cyanobacteria <scp>UCYN</scp>‐<scp>A</scp> and its prymnesiophyte host

Thompson, Anne; Carter, Brandon J.; Turk‐Kubo, Kendra A.; Malfatti, Francesca; Azam, Farooq; Zehr, Jonathan P.

doi:10.1111/1462-2920.12490

Cited by 121 publications

(284 citation statements)

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“…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.…”

Section: Arafura Sea Coral Seasupporting

confidence: 88%

“…It must be noted that amplicon sequencing approaches can only reconcile relative abundances and therefore do not allow for the absolute quantification of colonial versus singlecelled diazotrophs and that it is difficult to directly equate diazotroph communities to N 2 fixation activity. However, we identified a range of photoautotrophic, photoheterotrophic and heterotrophic bacteria that share high similarities in nifH sequences to those recovered from similar oceanic environments (for example, Langlois et al, 2005;Moisander et al, 2010;Bombar et al, 2013;Moisander et al, 2014;Thompson et al, 2014).…”

Section: Discussionmentioning

confidence: 95%

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

et al. 2015

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Australia's tropical waters represent predicted 'hotspots' for nitrogen (N 2 ) fixation based on empirical and modelled data. However, the identity, activity and ecology of diazotrophs within this region are virtually unknown. By coupling DNA and cDNA sequencing of nitrogenase genes (nifH) with sizefractionated N 2 fixation rate measurements, we elucidated diazotroph dynamics across the shelf region of the Arafura and Timor Seas (ATS) and oceanic Coral Sea during Austral spring and winter. During spring, Trichodesmium dominated ATS assemblages, comprising 60% of nifH DNA sequences, while Candidatus Atelocyanobacterium thalassa (UCYN-A) comprised 42% in the Coral Sea. In contrast, during winter the relative abundance of heterotrophic unicellular diazotrophs (δ-proteobacteria and γ-24774A11) increased in both regions, concomitant with a marked decline in UCYN-A sequences, whereby this clade effectively disappeared in the Coral Sea. Conservative estimates of N 2 fixation rates ranged from o1 to 91 nmol l − 1 day − 1 , and size fractionation indicated that unicellular organisms dominated N 2 fixation during both spring and winter, but average unicellular rates were up to 10-fold higher in winter than in spring. Relative abundances of UCYN-A1 and γ-24774A11 nifH transcripts negatively correlated to silicate and phosphate, suggesting an affinity for oligotrophy. Our results indicate that Australia's tropical waters are indeed hotspots for N 2 fixation and that regional physicochemical characteristics drive differential contributions of cyanobacterial and heterotrophic phylotypes to N 2 fixation.

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Section: Arafura Sea Coral Seasupporting

confidence: 88%

Section: Discussionmentioning

confidence: 95%

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

et al. 2015

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“…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). 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).…”

Section: Discussionmentioning

confidence: 58%

“…Later, endosymbiotic UCYN-A was also discovered in B. bigelowii by transmission electron microscopic observations (Hagino et al, 2013). Phylogenetic analyses using the UCYN-A nitrogenase (nifH) gene revealed at least three distinct clades, UCYN-A1, -A2 and -A3 (Thompson et al, 2014), and highlighted specificity between host and symbiont pairings, suggesting co-evolution between symbionts and hosts Thompson et al, 2014). Thus the clade UCYN-A1 was associated with an open ocean small prymnesiophyte (hereafter UCYN-A1 host), and the clade UCYN-A2 was associated with the coastal and larger B. bigelowii (hereafter UCYN-A2 host), while no host has been yet proposed for UCYN-A3.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2015

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A marine symbiosis has been recently discovered between prymnesiophyte species and the unicellular diazotrophic cyanobacterium UCYN-A. At least two different UCYN-A phylotypes exist, the clade UCYN-A1 in symbiosis with an uncultured small prymnesiophyte and the clade UCYN-A2 in symbiosis with the larger Braarudosphaera bigelowii. We targeted the prymnesiophyte-UCYN-A1 symbiosis by double CARD-FISH (catalyzed reporter deposition-fluorescence in situ hybridization) and analyzed its abundance in surface samples from the MALASPINA circumnavigation expedition. Our use of a specific probe for the prymnesiophyte partner allowed us to verify that this algal species virtually always carried the UCYN-A symbiont, indicating that the association was also obligate for the host. The prymnesiophyte-UCYN-A1 symbiosis was detected in all ocean basins, displaying a patchy distribution with abundances (up to 500 cells ml − 1 ) that could vary orders of magnitude. Additional vertical profiles taken at the NE Atlantic showed that this symbiosis occupied the upper water column and disappeared towards the Deep Chlorophyll Maximum, where the biomass of the prymnesiophyte assemblage peaked. Moreover, sequences of both prymnesiophyte partners were searched within a large 18S rDNA metabarcoding data set from the Tara-Oceans expedition around the world. This sequence-based analysis supported the patchy distribution of the UCYN-A1 host observed by CARD-FISH and highlighted an unexpected homogeneous distribution (at low relative abundance) of B. bigelowii in the open ocean. Our results demonstrate that partners are always in symbiosis in nature and show contrasted ecological patterns of the two related lineages.

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Contrasted geographical distribution of N₂ fixation rates and nifH phylotypes in the Coral and Solomon Seas (southwestern Pacific) during austral winter conditions

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Turk‐Kubo

et al. 2015

Global Biogeochemical Cycles

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Biological dinitrogen (N2) fixation and the distribution of diazotrophic phylotypes were investigated during two cruises in the Coral Sea and the Solomon Sea (southwestern Pacific) during austral winter conditions. N2 fixation rates were measurable at every station, but integrated (0–150 m) rates were an order of magnitude higher in the Solomon Sea (30 to 5449 µmol N m−2 d−1) compared to those measured in the Coral Sea (2 to 109 µmol N m−2 d−1). Rates measured in the Solomon Sea were in the upper range (100–1000 µmol N m−2 d−1) or higher than rates compiled in the global MARine Ecosystem biomass DATa database, indicating that this region has some of the highest N2 fixation rates reported in the global ocean. While unicellular diazotrophic cyanobacteria from group A (UCYN‐A1 and UCYN‐A2) and the proteobacteria γ‐24774A11 dominated in the Coral Sea and were correlated with N2 fixation rates (p < 0.05), Trichodesmium and UCYN‐B dominated in the Solomon Sea and were correlated (p < 0.05) with N2 fixation rates. UCYN‐A were totally absent in the Solomon Sea. The biogeographical distribution of diazotrophs is discussed within the context of patterns in measured environmental parameters.

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Genetic diversity of the unicellular nitrogen‐fixing cyanobacteria UCYN‐A and its prymnesiophyte host

Abstract: Summary 21Symbiotic interactions between nitrogen-fixing prokaryotes and photosynthetic

Cited by 121 publications

References 59 publications

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

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

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

Contrasted geographical distribution of N₂ fixation rates and nifH phylotypes in the Coral and Solomon Seas (southwestern Pacific) during austral winter conditions

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Genetic diversity of the unicellular nitrogen‐fixing cyanobacteria UCYN‐A and its prymnesiophyte host

Abstract: Summary 21Symbiotic interactions between nitrogen-fixing prokaryotes and photosynthetic

Cited by 121 publications

References 59 publications

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

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

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

Contrasted geographical distribution of N2 fixation rates and nifH phylotypes in the Coral and Solomon Seas (southwestern Pacific) during austral winter conditions

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Contrasted geographical distribution of N₂ fixation rates and nifH phylotypes in the Coral and Solomon Seas (southwestern Pacific) during austral winter conditions