Bacterial degradation of sinking diatom aggregates is key for the availability of organic matter in the deep-ocean. Yet, little is known about the impact of aggregate colonization by different ...bacterial taxa on organic carbon and nutrient cycling within aggregates. Here, we tracked the carbon (C) and nitrogen (N) transfer from the diatom Leptocylindrus danicus to different environmental bacterial groups using a combination of
C and
N isotope incubation (incubated for 72 h), CARD-FISH and nanoSIMS single-cell analysis. Pseudoalteromonas bacterial group was the first colonizing diatom-aggregates, succeeded by the Alteromonas group. Within aggregates, diatom-attached bacteria were considerably more enriched in
C and
N than non-attached bacteria. Isotopic mass balance budget indicates that both groups showed comparable levels of diatom C in their biomass, accounting for 19 ± 7% and 15 ± 11%, respectively. In contrast to C, bacteria of the Alteromonas groups showed significantly higher levels of N derived from diatoms (77 ± 28%) than Pseudoalteromonas (47 ± 17%), suggesting a competitive advantage for Alteromonas in the N-limiting environments of the deep-sea. Our results imply that bacterial succession within diatom aggregates may largely impact taxa-specific C and N uptake, which may have important consequences for the quantity and quality of organic matter exported to the deep ocean.
Dinitrogen (N2) fixation was investigated together with organic matter composition in the mesopelagic zone of the Bismarck (Transect 1) and Solomon (Transect 2) Seas (Southwest Pacific). Transparent ...exopolymer particles (TEP) and the presence of compounds sharing molecular formulae with saturated fatty acids and sugars, as well as dissolved organic matter (DOM) compounds containing nitrogen (N) and phosphorus (P) were higher on Transect 1 than on Transect 2, while oxygen concentrations showed an opposite pattern. N2 fixation rates (up to ~1 nmol N L-1 d-1) were higher in Transect 1 than in Transect 2, and correlated positively with TEP, suggesting a dependence of diazotroph activity on organic matter. The scores of the multivariate ordination of DOM molecular formulae and their relative abundance correlated negatively with bacterial abundances and positively with N2 fixation rates, suggesting an active bacterial exploitation of DOM and its use to sustain diazotrophic activity. Sequences of the nifH gene clustered with Alpha-, Beta-, Gamma- and Deltaproteobacteria, and included representatives from Clusters I, III and IV. A third of the clone library included sequences close to the potentially anaerobic Cluster III, suggesting that N2 fixation was partially supported by presumably particle-attached diazotrophs. Quantitative polymerase chain reaction (qPCR) primer-probe sets were designed for three phylotypes and showed low abundances, with a phylotype within Cluster III at up to 103 nifH gene copies L-1. These results provide new insights into the ecology of non-cyanobacterial diazotrophs and suggest that organic matter sustains their activity in the mesopelagic ocean.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
N2 fixation rates were measured daily in large (∼ 50 m3) mesocosms deployed in the tropical southwest Pacific coastal ocean (New Caledonia) to investigate the temporal variability in N2 fixation ...rates in relation with environmental parameters and study the fate of diazotroph-derived nitrogen (DDN) in a low-nutrient, low-chlorophyll ecosystem. The mesocosms were fertilized with ∼ 0.8 µM dissolved inorganic phosphorus (DIP) to stimulate diazotrophy. Bulk N2 fixation rates were replicable between the three mesocosms, averaged 18.5 ± 1.1 nmol N L−1 d−1 over the 23 days, and increased by a factor of 2 during the second half of the experiment (days 15 to 23) to reach 27.3 ± 1.0 nmol N L−1 d−1. These later rates measured after the DIP fertilization are higher than the upper range reported for the global ocean. During the 23 days of the experiment, N2 fixation rates were positively correlated with seawater temperature, primary production, bacterial production, standing stocks of particulate organic carbon (POC), nitrogen (PON) and phosphorus (POP), and alkaline phosphatase activity, and negatively correlated with DIP concentrations, DIP turnover time, nitrate, and dissolved organic nitrogen and phosphorus concentrations. The fate of DDN was investigated during a bloom of the unicellular diazotroph UCYN-C that occurred during the second half of the experiment. Quantification of diazotrophs in the sediment traps indicates that ∼ 10 % of UCYN-C from the water column was exported daily to the traps, representing as much as 22.4 ± 5.5 % of the total POC exported at the height of the UCYN-C bloom. This export was mainly due to the aggregation of small (5.7 ± 0.8 µm) UCYN-C cells into large (100–500 µm) aggregates. During the same time period, a DDN transfer experiment based on high-resolution nanometer-scale secondary ion mass spectrometry (nanoSIMS) coupled with 15N2 isotopic labeling revealed that 16 ± 6 % of the DDN was released to the dissolved pool and 21 ± 4 % was transferred to non-diazotrophic plankton, mainly picoplankton (18 ± 4 %) followed by diatoms (3 ± 2 %). This is consistent with the observed dramatic increase in picoplankton and diatom abundances, primary production, bacterial production, and standing stocks of POC, PON, and POP in the mesocosms during the second half of the experiment. These results offer insights into the fate of DDN during a bloom of UCYN-C in low-nutrient, low-chlorophyll ecosystems.
Nitrogen is essential for life but is often a major limiting nutrient for growth in the ocean. Biological dinitrogen fixation is a major source of new nitrogen to surface waters and promotes marine ...productivity. Yet the fate of diazotroph-derived nitrogen (DDN) in marine ecosystems has been poorly studied, and its transfer to auto- and heterotrophic plankton has not been measured. Here, we use high-resolution nanometer scale secondary ion mass spectrometry (nanoSIMS) coupled with 15N₂ isotopic labelling and flow cytometry cell sorting to examine the DDN transfer to specific groups of natural phytoplankton and bacteria during three diazotroph blooms dominated by the cyanobacterium Trichodesmium spp. in the South West Pacific. During these experiments, 13%±2% to 48%±5% of the fixed 15N₂ was released into the dissolved pool and 6%±1% to 8%±2% of this DDN was transferred to non-diazotrophic plankton after 48 h. The primary beneficiaries of this DDN were diatoms (45%±4% to 61%±38%) and bacteria (22%±27% to 38%±12%), followed by pico-phytoplankton (3%±1% to 21%±14%). The DDN was quickly converted to non-diazotrophic plankton biomass, in particular that of diatoms, which increased in abundance by a factor of 1.4–15 over the course of the three experiments. The single-cell approach we used enabled quantification of the actual transfer of DDN to specific groups of autotrophic and heterotrophic plankton in the surface ocean, revealing a previously unseen level of complexity in the pathways that occur between N₂ fixation and the eventual export of DDN from the photic zone.
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.
We performed nitrogen (N) budgets in the photic layer of three
contrasting stations representing different trophic conditions in the western
tropical South Pacific (WTSP) Ocean during austral summer ...conditions
(February–March 2015). Using a Lagrangian strategy, we sampled the same
water mass for the entire duration of each long-duration (5 days) station,
allowing us to consider only vertical exchanges for the budgets. We
quantified all major vertical N fluxes both entering (N2 fixation,
nitrate turbulent diffusion, atmospheric deposition) and leaving the photic
layer (particulate N export). The three stations were characterized by a
strong nitracline and contrasted deep chlorophyll maximum depths, which were
lower in the oligotrophic Melanesian archipelago (MA, stations LD A and LD B)
than in the ultra-oligotrophic waters of the South Pacific Gyre (SPG, station
LD C). N2 fixation rates were extremely high at both LD A
(593 ± 51 µmol N m−2 d−1) and LD B
(706 ± 302 µmol N m−2 d−1), and the diazotroph
community was dominated by Trichodesmium. N2 fixation rates
were lower (59 ± 16 µmol N m−2 d−1) at LD C, and
the diazotroph community was dominated by unicellular N2-fixing
cyanobacteria (UCYN). At all stations, N2 fixation was the major source
of new N (> 90 %) before atmospheric deposition and upward nitrate
fluxes induced by turbulence. N2 fixation contributed circa 13–18 %
of primary production in the MA region and 3 % in the
SPG water and sustained
nearly all new primary production at all stations. The e ratio
(e ratio = particulate carbon export ∕ primary production) was
maximum at LD A (9.7 %) and was higher than the e ratio in most studied
oligotrophic regions (< 5 %), indicating a high efficiency of the WTSP
to export carbon relative to primary production. The direct export of
diazotrophs assessed by qPCR of the nifH gene in sediment traps
represented up to 30.6 % of the PC export at LD A, while their
contribution was 5 and < 0.1 % at LD B and LD C, respectively. At the
three studied stations, the sum of all N input to the photic layer exceeded
the N output through organic matter export. This disequilibrium leading to N
accumulation in the upper layer appears as a characteristic of the WTSP
during the summer season.
In marine ecosystems, biological N2 fixation provides the predominant external source of nitrogen (N; 140 ± 50 Tg N yr−1), contributing more than atmospheric and riverine inputs to the N supply. Yet ...the fate and magnitude of the newly fixed N, or diazotroph-derived N (hereafter named DDN) in marine ecosystems is poorly understood. Moreover, whether the DDN is preferentially and directly exported out of the photic zone, recycled by the microbial loop and/or transferred into larger organisms remains unclear. These questions were investigated in the framework of the VAHINE (VAriability of vertical and tropHIc transfer of diazotroph derived N in the south wEst Pacific) project. Triplicate large volume ( ∼ 50 m3) mesocosms were deployed in the tropical south-west Pacific coastal ocean (New Caledonia). The mesocosms were intentionally fertilized with ∼ 0.8 µM dissolved inorganic phosphorus (DIP) at the start of the experiment to stimulate diazotrophy. A total of 47 stocks, fluxes, enzymatic activities and diversity parameters were measured daily inside and outside the mesocosms by the 40 scientists involved in the project. The experiment lasted for 23 days and was characterized by two distinct and successive diazotroph blooms: a dominance of diatom-diazotroph associations (DDAs) during the first half of the experiment (days 2–14) followed by a bloom of unicellular cyanobacterial lineage C (UCYN-C during the second half of the experiment (days 15–23). These conditions provided a unique opportunity to compare the DDN transfer and export efficiency associated with different diazotrophs. Here we summarize the major experimental and modelling results obtained during the project and described in the VAHINE special issue, in particular those regarding the evolution of the main standing stocks, fluxes and biological characteristics over the 23-day experiment, the contribution of N2 fixation to export fluxes, the DDN released to dissolved pool and its transfer to the planktonic food web (bacteria, phytoplankton, zooplankton). We then apply our Eco3M modelling platform to further infer the fate of DDN in the ecosystem and the role of N2 fixation on productivity, food web structure and carbon export. Recommendations for future work are finally provided in the conclusion section.
Nitrogen (N) is the building block of life. Quantifying the sources and sinks of N to the ocean is essential for predicting its productivity and potential carbon sequestration. In his paper, Gruber ...(1) seeks for “elusive marine nitrogen fixation” following results from Knapp et al. (2), who measured unexpectedly low N input through N2 fixation in the eastern tropical South Pacific (ETSP), seriously bringing into question the proposed close spatial coupling between N input (through N2 fixation) and loss (through denitrification) (3). Here, we compile data from recently published and unpublished studies revealing a hot spot of N2 fixation in the western tropical South Pacific (WTSP) arguing for a spatial decoupling between N sources and sinks in the South Pacific.
The globally distributed diazotroph Trichodesmium contributes importantly to nitrogen inputs in the oligotrophic oceans. Sites of dissolved organic matter (DOM) accumulation could promote the ...mixotrophic nutrition of Trichodesmium when inorganic nutrients are scarce. Nano-scale secondary ion mass spectrometry (nanoSIMS) analyses of individual trichomes sampled in the South Pacific Ocean, showed significant
C-enrichments after incubation with either
C-labeled carbohydrates or amino acids. These results suggest that DOM could be directly taken up by Trichodesmium or primarily consumed by heterotrophic epibiont bacteria that ultimately transfer reduced DOM compounds to their host trichomes. Although the addition of carbohydrates or amino acids did not significantly affect bulk N
fixation rates, N
fixation was enhanced by amino acids in individual colonies of Trichodesmium. We discuss the ecological advantages of DOM use by Trichodesmium as an alternative to autotrophic nutrition in oligotrophic open ocean waters.
Dinitrogen (N2) fixation rates were investigated in the euphotic layer of the Bismarck and Solomon Seas using 15N2 incubation assays taking into account both the particulate and the dissolved pools. ...Average depth‐integrated particulate N2 fixation rates were 203 (range 43–399) and 1396 (range 176–3132) μmol N m−2 d−1 in the Bismarck and Solomon Seas, respectively. In both seas, N2 fixation measured in the dissolved pool was similar to particulate N2 fixation, highlighting the potentially substantial underestimation of N2 fixation in oceanic budgets when only particulate N2 fixation is considered. Among the diazotroph phylotypes targeted using quantitative polymerase chain reaction amplification of nifH genes, Trichodesmium was the most abundant. Regression analyses suggest that it accounted for the major proportion of N2 fixation. However, unicellular cyanobacterial and non‐cyanobacterial diazotrophs were also occasionally abundant. This study reports high pelagic N2 fixation rates and confirms that the Western Tropical South Pacific is a hot spot for marine N2 fixation.
Key Points
The Bismarck and Solomon Seas are hot spots of dinitrogen fixation in the ocean
Dinitrogen fixation is underestimated if the dissolved pool is not taken into account
Regression analyses indicate that most of the dinitrogen fixation activity is attributed to Trichodesmium
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