Abstract. The abundance and distribution of cyanobacterial diazotrophs were quantified in two regions (Melanesian archipelago, MA; and subtropical gyre, SG) of the western tropical South Pacific using nifH quantitative polymerase chain reaction (qPCR) assays. UCYN-A1 and A2 host populations were quantified using 18S rRNA qPCR assays including one newly developed assay. All phylotypes were detected in the upper photic zone (0–50 m), with higher abundances in the MA region. Trichodesmium and UCYN-B dominated and ranged from 2.18 × 102 to 9.41 × 106 and 1.10 × 102 to 2.78 × 106 nifH copies L−1, respectively. Het-1 (symbiont of Rhizosolenia diatoms) was the next most abundant (1.40 × 101–1.74 × 105 nifH copies L−1) and co-occurred with het-2 and het-3. UCYN-A1 and A2 were the least abundant diazotrophs and were below detection (bd) in 63 and 79, respectively, of 120 samples. In addition, in up to 39 % of samples in which UCYN-A1 and A2 were detected, their respective hosts were bd. Pairwise comparisons of the nifH abundances and various environmental parameters supported two groups: a deep-dwelling group (45 m) comprised of UCYN-A1 and A2 and a surface group (0–15 m) comprised of Trichodesmium, het-1 and het-2. Temperature and photosynthetically active radiation were positively correlated with the surface group, while UCYN-A1 and A2 were positively correlated with depth, salinity, and oxygen. Similarly, in a meta-analysis of 11 external datasets, all diazotrophs, except UCYN-A were correlated with temperature. Combined, our results indicate that conditions favoring the UCYN-A symbiosis differ from those of diatom diazotroph associations and free-living cyanobacterial diazotrophs.
Abstract. Here we report N2 fixation rates from a ∼ 4000 km transect in the western and central tropical South Pacific, a particularly undersampled region in the world ocean. Water samples were collected in the euphotic layer along a west to east transect from 160∘ E to 160∘ W that covered contrasting trophic regimes, from oligotrophy in the Melanesian archipelago (MA) waters to ultra-oligotrophy in the South Pacific Gyre (GY) waters. N2 fixation was detected at all 17 sampled stations with an average depth-integrated rate of 631 ± 286 µmolNm-2d-1 (range 196–1153 µmolNm-2d-1) in MA waters and of 85 ± 79 µmolNm-2d-1 (range 18–172 µmolNm-2d-1) in GY waters. Two cyanobacteria, the larger colonial filamentous Trichodesmium and the smaller UCYN-B, dominated the enumerated diazotroph community (> 80 %) and gene expression of the nifH gene (cDNA > 105 nifH copies L−1) in MA waters. Single-cell isotopic analyses performed by nanoscale secondary ion mass spectrometry (nanoSIMS) at selected stations revealed that Trichodesmium was always the major contributor to N2 fixation in MA waters, accounting for 47.1–83.8 % of bulk N2 fixation. The most plausible environmental factors explaining such exceptionally high rates of N2 fixation in MA waters are discussed in detail, emphasizing the role of macro- and micro-nutrient (e.g., iron) availability, seawater temperature and currents.
1The abundance and distribution of cyanobacterial diazotrophs were quantified in two regions 2 (Melanesian archipelago, MA and subtropical gyre, SG) of the Western Tropical South 3 Pacific using nifH qPCR assays. UCYN-A1 and A2 host populations were quantified using 4 18S rRNA qPCR assays including one newly developed assay. All phylotypes were detected
1Here we report quantification of N2 fixation rates over a ~4000 km transect in the western and central tropical South ) in MA waters, 9and single-cell isotopic analyses performed by nanoscale secondary ion mass spectrometry at selected stations reveal 10that Trichodesmium was always the major contributor to N2 fixation in MA waters, accounting for 47.1 to 83.8 % of 11 bulk N2 fixation. 1In the ocean, nitrogen (N) availability in surface waters controls primary production and export of organic matter 2 (Dugdale and Goering, 1967; Eppley and Peterson, 1979; Moore et al., 2013), a process commonly referred to as 'the 3 biological carbon pump'. The major external source of new N to the ocean is biological N2 fixation (100-150 Tg N yr -4 1 , (Gruber, 2008)), the conversion of N2 gas dissolved in seawater into ammonia (NH4 + ). This process is performed by 5 diazotrophic organisms possessing the enzyme nitrogenase encoded by the nifH genes. This source is continuously 6 counteracted by N losses, mainly driven by denitrification and anammox, which convert fixed N (nitrate, NO3 -) into 7 N2. Despite the critical importance of the N inventory in regulating primary production and export, the spatial 8 distribution of N gains and losses in the ocean is still poorly resolved. 9A global scale modeling study predicted that the highest rates of N2 fixation are located in the South Pacific 10Ocean (Deutsch et al., 2007; Gruber, 2016). These authors also concluded that processes leading to N gains and losses 11are spatially coupled to oxygen deficient zones such as in the eastern tropical Pacific (ETSP), which harbors NO3 -- 12poor but phosphate-rich surface waters, i.e. potentially ideal niches for N2 fixation (Monteiro et al., 2011). However, 13recent field studies based on several cruises and independent approaches, including biological 15the surface ETSP waters (Dekaezemacker et al., 2013; Fernandez et al., 2011; Fernandez et al., 2015; Knapp et al., 16 2016; Loescher et al., 2014), presumably due to iron (Fe) limitation (Bonnet et al., 2017; Dekaezemacker et al., 2013), 17as Fe is a major component of the nitrogenase enzyme (Raven, 1988). On the opposite, the western tropical South 18Pacific (WTSP) has recently been identified as a 'hot spot' of N2 fixation (Bonnet et al., 2017) and together, these 19 studies plead for a basin-wide spatial decoupling between N2 fixation and denitrification in the South Pacific Ocean. 20The WTSP is a vast oceanic region extending from Australia in the west to the western boundary of the South 21Pacific Gyre in the east (hereafter referred to as GY waters) ( Figure 1). It has been chronically undersampled (Luo et 22 al., 2012) compared to the tropical North Atlantic (Benavides and Voss, 2015) and North Pacific (e.g. (Böttjer et al., 23 2017)) oceans, but recent oceanographic surveys performed in the western part of the WTSP, in the Solomon, Bismarck 24 (Berthelot et al., 2017; Bonnet et al., 2009; Bonnet et al., 2015) and Arafura (Messer et al., 2016; Montoya et al.,...
Diatom diazotroph associations (DDAs) are important components in the world’s oceans, especially in the western tropical north Atlantic (WTNA), where blooms have a significant impact on carbon and nitrogen cycling. However, drivers of their abundances and distribution patterns remain unknown. Here, we examined abundance and distribution patterns for two DDA populations in relation to the Amazon River (AR) plume in the WTNA. Quantitative PCR assays, targeting two DDAs (het-1 and het-2) by their symbiont’s nifH gene, served as input in a piecewise structural equation model (SEM). Collections were made during high (spring 2010) and low (fall 2011) flow discharges of the AR. The distributions of dissolved nutrients, chlorophyll-a, and DDAs showed coherent patterns indicative of areas influenced by the AR. A symbiotic Hemiaulus hauckii-Richelia (het-2) bloom (>106 cells L-1) occurred during higher discharge of the AR and was coincident with mesohaline to oceanic (30–35) sea surface salinities (SSS), and regions devoid of dissolved inorganic nitrogen (DIN), low concentrations of both DIP (>0.1 μmol L-1) and Si (>1.0 μmol L-1). The Richelia (het-1) associated with Rhizosolenia was only present in 2010 and at lower densities (10-1.76 × 105 nifH copies L-1) than het-2 and limited to regions of oceanic SSS (>36). The het-2 symbiont detected in 2011 was associated with H. membranaceus (>103 nifH copies L-1) and were restricted to regions with mesohaline SSS (31.8–34.3), immeasurable DIN, moderate DIP (0.1–0.60 μmol L-1) and higher Si (4.19–22.1 μmol L-1). The piecewise SEM identified a profound direct negative effect of turbidity on the het-2 abundance in spring 2010, while DIP and water turbidity had a more positive influence in fall 2011, corroborating our observations of DDAs at subsurface maximas. We also found a striking difference in the influence of salinity on DDA symbionts suggesting a niche differentiation and preferences in oceanic and mesohaline salinities by het-1 and het-2, respectively. The use of the piecewise SEM to disentangle the complex and concomitant hydrography of the WTNA acting on two biogeochemically relevant populations was novel and underscores its use to predict conditions favoring abundance and distributions of microbial populations.
Abstract. The fate of diazotroph (N2 fixers) derived carbon (C) and nitrogen (N) and their contribution to vertical export of C and N in the western tropical South Pacific Ocean was studied during OUTPACE (Oligotrophy to UlTra-oligotrophy PACific Experiment). Our specific objective during OUTPACE was to determine whether autocatalytic programmed cell death (PCD), occurring in some diazotrophs, is an important mechanism affecting diazotroph mortality and a factor regulating the vertical flux of organic matter and, thus, the fate of the blooms. We sampled at three long duration (LD) stations of 5 days each (LDA, LDB and LDC) where drifting sediment traps were deployed at 150, 325 and 500 m depth. LDA and LDB were characterized by high chlorophyll a (Chl a) concentrations (0.2–0.6 µg L−1) and dominated by dense biomass of the filamentous cyanobacterium Trichodesmium as well as UCYN-B and diatom–diazotroph associations (Rhizosolenia with Richelia-detected by microscopy and het-1 nifH copies). Station LDC was located at an ultra-oligotrophic area of the South Pacific gyre with extremely low Chl a concentration (∼ 0.02 µg L−1) with limited biomass of diazotrophs predominantly the unicellular UCYN-B. Our measurements of biomass from LDA and LDB yielded high activities of caspase-like and metacaspase proteases that are indicative of PCD in Trichodesmium and other phytoplankton. Metacaspase activity, reported here for the first time from oceanic populations, was highest at the surface of both LDA and LDB, where we also obtained high concentrations of transparent exopolymeric particles (TEP). TEP were negatively correlated with dissolved inorganic phosphorus and positively coupled to both the dissolved and particulate organic carbon pools. Our results reflect the increase in TEP production under nutrient stress and its role as a source of sticky carbon facilitating aggregation and rapid vertical sinking. Evidence for bloom decline was observed at both LDA and LDB. However, the physiological status and rates of decline of the blooms differed between the stations, influencing the amount of accumulated diazotrophic organic matter and mass flux observed in the traps during our experimental time frame. At LDA sediment traps contained the greatest export of particulate matter and significant numbers of both intact and decaying Trichodesmium, UCYN-B and het-1 compared to LDB where the bloom decline began only 2 days prior to leaving the station and to LDC where no evidence for bloom or bloom decline was seen. Substantiating previous findings from laboratory cultures linking PCD to carbon export in Trichodesmium, our results from OUTPACE indicate that nutrient limitation may induce PCD in high biomass blooms such as displayed by Trichodesmium or diatom–diazotroph associations. Furthermore, PCD combined with high TEP production will tend to facilitate cellular aggregation and bloom termination and will expedite vertical flux to depth.
Some N 2 -fixing cyanobacteria form symbiosis with diverse protists. In the plankton two groups of diazotrophic symbioses are described: (1) a collective group of diatoms which associate with heterocystous cyanobacteria (Diatom Diazotroph Associations, DDA), and (2) the microalgal prymnesiophyte Braarudosphaera bigelowii and its relatives which associate with the unicellular cyanobacterium Candidatus Atelocyanobacterium thalassa (hereafter as UCYN-A). Both symbiotic systems co-occur, and in both partnerships the symbionts function as a nitrogen (N) source. In this perspective, we provide a brief comparison between the DDAs and the prymnesiophyte-UCYN-A symbioses highlighting similarities and differences in both systems, and present a bias in the attention and current methodology that has led to an under-detection and under-estimation of the DDAs.
27The fate of diazotroph (N2 fixers) derived carbon (C) and nitrogen (N) and their contribution to vertical 28 export of C and N in the Western Tropical South Pacific Ocean was studied in OUTPACE (Oligotrophy 29to UlTra-oligotrophy PACific Experiment). Our specific objective during OUTPACE was to determine 30 whether autocatalytic programmed cell death (PCD) is an important mechanism affecting diazotroph 31 mortality and a factor regulating the vertical flux of organic matter and thus the fate of the blooms. We 32 sampled at three long duration (LD
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