Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre

Halm, Hannah; Lam, Phyllis; Ferdelman, Timothy G.; Lavik, Gaute; Dittmar, Thorsten; LaRoche, Julie; Dhondt, Steven; Kuypers, Marcel M. M.

doi:10.1038/ismej.2011.182

Cited by 181 publications

(248 citation statements)

References 52 publications

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“…Conversely, Coral Sea communities contained a greater diversity of cyanobacterial phylotypes, including ecotypes of UCYN-A, alongside a lower frequency of Trichodesmium sequences, as well as heterotrophic diazotrophs. The composition of Coral Sea diazotroph populations appears similar to those found within the wider tropical and subtropical South Pacific (Moisander et al, 2010(Moisander et al, , 2014Halm et al, 2012). However, a seasonal shift in the composition of Coral Sea populations was also observed, such that the relative abundance of UCYN-A ecotypes decreased while γ-24774A11 increased between spring and winter, respectively.…”

Section: Arafura Sea Coral Seasupporting

confidence: 66%

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: 66%

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

et al. 2015

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“…Very high abundances of the D0CY3 (up to 3.3 Â 10 6 copies l À 1 ) and ECI27 (up to 2.2 Â 10 7 copies l À 1 ) clusters were observed at and below the chemocline (Figure 4 and Supplementary Table S3). These abundances are among the highest reported (but see Halm et al, 2012;Mulholland et al, 2012) and magnitudes higher than previous reports on cluster III phylotypes in the Pacific and Atlantic oceans (Church et al, 2005;Langlois et al, 2008). The activity of anaerobic N 2 -fixers is largely unknown but interestingly, transcripts of a cluster III phylotype were recently quantified to 1.9 Â 10 3 copies l À 1 at 200 m in the South Pacific Gyre (Halm et al, 2012).…”

Section: Distribution and Abundances Of Nifh Phylotypes And Transcriptsmentioning

confidence: 65%

“…These abundances are among the highest reported (but see Halm et al, 2012;Mulholland et al, 2012) and magnitudes higher than previous reports on cluster III phylotypes in the Pacific and Atlantic oceans (Church et al, 2005;Langlois et al, 2008). The activity of anaerobic N 2 -fixers is largely unknown but interestingly, transcripts of a cluster III phylotype were recently quantified to 1.9 Â 10 3 copies l À 1 at 200 m in the South Pacific Gyre (Halm et al, 2012). In our study, transcripts of D0CY3 (3.2 Â 10 4 and 6.5 Â 10 3 copies l À 1 ) at the two consecutive samplings for 200 m Gotland Deep samples (Figure 4 and Supplementary Table S3) and the co-occurrence of genes and transcripts also at the Bornholm Basin (88 m, Figure 5) further highlights the potential significance of cluster III phylotypes as N 2 -fixers in suboxic/anoxic waters.…”

Section: Distribution and Abundances Of Nifh Phylotypes And Transcriptsmentioning

confidence: 78%

Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea

et al. 2013

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The Baltic Sea receives large nitrogen inputs by diazotrophic (N 2 -fixing) heterocystous cyanobacteria but the significance of heterotrophic N 2 fixation has not been studied. Here, the diversity, abundance and transcription of the nifH fragment of the nitrogenase enzyme in two basins of the Baltic Sea proper was examined. N 2 fixation was measured at the surface (5 m) and in anoxic water (200 m). Vertical sampling profiles of 410 and o10 lm size fractions were collected in 2007, 2008 and 2011 at the Gotland Deep and in 2011 in the Bornholm Basin. Both of these stations are characterized by permanently anoxic bottom water. The 454-pyrosequencing nifH analysis revealed a diverse assemblage of nifH genes related to alpha-, beta-and gammaproteobacteria (nifH cluster I) and anaerobic bacteria (nifH cluster III) at and below the chemocline. Abundances of genes and transcripts of seven diazotrophic phylotypes were investigated using quantitative polymerase chain reaction revealing abundances of heterotrophic nifH phylotypes of up to 2.1 Â 10 7 nifH copies l À 1 . Abundant nifH transcripts (up to 3.2 Â 10 4 transcripts l À 1 ) within nifH cluster III and co-occurring N 2 fixation (0.44 ± 0.26 nmol l À 1 day À 1 ) in deep water suggests that heterotrophic diazotrophs are fixing N 2 in anoxic ammonium-rich waters. Our results reveal that N 2 fixation in the Baltic Sea is not limited to illuminated N-deplete surface waters and suggest that N 2 fixation could also be of importance in other suboxic regions of the world's oceans. The ISME Journal (2013Journal ( ) 7, 1413Journal ( -1423 doi:10.1038/ismej.2013 published online 28 February 2013 Subject Category: microbial ecology and functional diversity of natural habitats

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“…These values were in the medium-high range of global abundances reviewed by Luo et al (2012), and by Benavides and Voss (2015) specifically from studies performed in the North Atlantic. In fact, heterotrophic diazotrophs abundances higher than 10 4 nifH copies L −1 have seldom been reported in the marine environment (e.g., Moisander et al, 2008;Halm et al, 2012). The abundance of the heterotrophic Gammaproteobacteria was positively correlated with temperature (Pearson's r = 0.473, p < 0.05) and mixed layer depth (Pearson's r = 0.495, p < 0.05), since slightly higher abundances were measured during downwelling conditions, when the water column was warmer, less stratified and probably depleted in bioessential nutrients.…”

Section: Playersmentioning

confidence: 99%

Biological N2 Fixation in the Upwelling Region off NW Iberia: Magnitude, Relevance, and Players

et al. 2017

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The classical paradigm about marine N 2 fixation establishes that this process is mainly constrained to nitrogen-poor tropical and subtropical regions, and sustained by the colonial cyanobacterium Trichodesmium spp. and diatom-diazotroph symbiosis. However, the application of molecular techniques allowed determining a high phylogenic diversity and wide distribution of marine diazotrophs, which extends the range of ocean environments where biological N 2 fixation may be relevant. Between February 2014 and December 2015, we carried out 10 one-day samplings in the upwelling system off NW Iberia in order to: (1) investigate the seasonal variability in the magnitude of N 2 fixation, (2) determine its biogeochemical role as a mechanism of new nitrogen supply, and (3) quantify the main diazotrophs in the region under contrasting hydrographic regimes. Our results indicate that the magnitude of N 2 fixation in this region was relatively low (0.001 ± 0.002 -0.095 ± 0.024 µmol N m −3 d −1 ), comparable to the lower-end of rates described for the subtropical NE Atlantic. Maximum rates were observed at the surface during both upwelling and relaxation conditions. The comparison with nitrate diffusive fluxes revealed the minor role of N 2 fixation (<2%) as a mechanism of new nitrogen supply into the euphotic layer. Small diazotrophs (<10 µm) were responsible for all N 2 fixation activity detected in the region. Quantitative PCR targeting the nifH gene revealed the highest abundances of two sublineages of Candidatus Atelocyanobacterium thalassa or UCYN-A (UCYN-A1 and UCYN-A2), mainly at surface waters during upwelling and relaxation conditions, and of Gammaproteobacteria γ-24774A11 at deep waters during downwelling. Maximum abundance for the three groups were up to 6.7 × 10 2 , 1.5 × 10 3 , and 2.4 × 10 4 nifH copies L −1 , respectively. Our findings demonstrate measurable N 2 fixation activity and presence of diazotrophs throughout the year in a nitrogen-rich temperate region.

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Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre

Cited by 181 publications

References 52 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

Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea

Biological N2 Fixation in the Upwelling Region off NW Iberia: Magnitude, Relevance, and Players

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