sophie bonnet - Academia.edu (original) (raw)

Papers by sophie bonnet

Research paper thumbnail of Diazotrophs are overlooked contributors to carbon and nitrogen export to the deep ocean

The ISME Journal

Diazotrophs are widespread microorganisms that alleviate nitrogen limitation in 60% of our oceans... more Diazotrophs are widespread microorganisms that alleviate nitrogen limitation in 60% of our oceans, thereby regulating marine productivity. Yet, the group-specific contribution of diazotrophs to organic matter export has not been quantified, which so far has impeded an accurate assessment of their impact on the biological carbon pump. Here, we examine the fate of five groups of globally-distributed diazotrophs by using an original combination of mesopelagic particle sampling devices across the subtropical South Pacific Ocean. We demonstrate that cyanobacterial and non-cyanobacterial diazotrophs are exported down to 1000 m depth. Surprisingly, group-specific export turnover rates point to a more efficient export of small unicellular cyanobacterial diazotrophs (UCYN) relative to the larger and filamentous Trichodesmium. Phycoerythrin-containing UCYN-B and UCYN-C-like cells were recurrently found embedded in large (>50 µm) organic aggregates or organized into clusters of tens to hund...

Research paper thumbnail of Dissolved organic matter stimulates N₂ fixation and nifH gene expression in Trichodesmium

FEMS Microbiology Letters, Apr 6, 2020

Mixotrophy, the combination of heterotrophic and autotrophic nutrition modes, is emerging as the ... more Mixotrophy, the combination of heterotrophic and autotrophic nutrition modes, is emerging as the rule rather than the exception in marine photosynthetic plankton. Trichodesmium, a prominent diazotroph ubiquitous in the (sub)tropical oceans, is generally considered to obtain energy via autotrophy. While the ability of Trichodesmium to use dissolved organic phosphorus when deprived of inorganic phosphorus sources is well known, the extent to which this important cyanobacterium may benefit from other dissolved organic matter (DOM) sources is unknown. Here we provide evidence of carbon-, nitrogen- and phosphorus-rich DOM molecules enhancing N₂ fixation rates and nifH gene expression in natural Trichodesmium colonies collected at two stations in the western tropical South Pacific. Sampling at a third station located in the oligotrophic South Pacific Gyre revealed no Trichodesmium but showed presence of UCYN-B, although no nifH expression was detected. Our results suggest that Trichodesmi...

Research paper thumbnail of Diazotroph community and activity in the Southern Indian Ocean

Research paper thumbnail of Insights into nitrogen fixation below the euphotic zone: trials in an oligotrophic marginal sea and global compilation

Nitrogen (N2) fixation, the energetically expensive conversion of N2 to ammonia, plays an importa... more Nitrogen (N2) fixation, the energetically expensive conversion of N2 to ammonia, plays an important role in balancing the global nitrogen budget. Defying historic paradigms, recent studies have detected non-cyanobacterial N2 fixation in deep, dark oceanic waters. Even low volumetric rates can be significant considering the large volume of these waters. However, measuring aphotic N2 fixation is an analytical challenge due to the low particulate nitrogen (PN) concentrations. Here, we investigated N2 fixation rates in aphotic waters in the South China Sea (SCS). To increase the sensitivity of N2 fixation rate measurements, we applied a novel approach requiring only 0.28 μg N for measuring the isotopic composition of particulate nitrogen. We conducted parallel 15 N2-enriched incubations in ambient seawater, seawater amended with amino acids and poisoned (HgCl2) controls, along with incubations that received no tracer additions to distinguish biological N2 fixation. Experimental treatments differed significantly from our two types of controls, those receiving no additions and killed controls. Amino acid additions masked N2 fixation signals due to the uptake of added 14 Namino acid. Results show that the maximum dark N2 fixation rates (1.28 ± 0.85 nmol N L-1 d-1) occurred within upper 200 m, while rates below 200 m were mostly lower than 0.1 nmol N L-1 d-1. Nevertheless, N2 fixation rates between 200 and 1000 m accounted for 39 ± 32 % of depth-integrated dark N2 fixation rates in the upper 1000 m, which is comparable to the areal nitrogen inputs via atmospheric deposition. Globally, we found that aphotic N2 fixation studies conducted in oxygenated environments yielded rates similar to those from the SCS (< 1 nmol N L-1 d-1), regardless of methods, while higher rates were occasionally observed in low-oxygen (< 62 µM) regions. Regression analysis suggests that particulate nitrogen concentrations could be a predictive proxy for detectable aphotic N2 fixation in the SCS and eastern tropical south Pacific.

Research paper thumbnail of Seasonal Shifts in Diazotrophs Players: Patterns Observed Over a Two-Year Time Series in the New Caledonian Lagoon (Western Tropical South Pacific Ocean)

Coastal and open ocean regions of the Western Tropical South Pacific ocean have been identified a... more Coastal and open ocean regions of the Western Tropical South Pacific ocean have been identified as a hotspot of N2 fixation. However, the environmental factors driving the temporal variability of abundance, composition, and activity of diazotrophs are still poorly understood, especially during the winter season. To address this, we quantified N2 fixation rates and the abundance of seven diazotroph phylotypes (UCYN-A1 symbiosis, UCYN-B, UCYN-C, Trichodesmium, Het-1, Het-2, and Het-3) on a monthly basis during two full years (2012 to 2014) at four stations along a coast to open ocean transect in the New Caledonian lagoon. The total nifH gene concentration (sum of all nifH gene copies) clearly decreased from the barrier reef to the shore. Apart from UCYN-B, which peaked at very high abundances (106–108 nifH gene copies L–1) at two occasions at the coastal station, the UCYN-A1 symbiosis was the most abundant group at all stations, accounting for 79% of the total nifH gene copy counts al...

Research paper thumbnail of Massive export of diazotrophs across the South Pacific tropical Ocean

bioRxiv, 2021

Diazotrophs are widespread microorganisms that alleviate nitrogen limitation in 60% of our oceans... more Diazotrophs are widespread microorganisms that alleviate nitrogen limitation in 60% of our oceans, regulating marine productivity. Yet, their contribution to organic matter export has not been quantified, making an assessment of their impact on the biological carbon pump impossible. Here, we demonstrate that cyanobacterial and non-cyanobacterial diazotrophs are massively exported down to 1000 m-depth in the western subtropical South Pacific Ocean (WTSP), accounting for up to 52-100% of the total particulate nitrogen export fluxes. We further demonstrate that small size unicellular diazotrophs (UCYN, 1-8 µm) are exported more efficiently than filamentous diazotrophs (>100-1000 µm) under the form of large (>50 µm) aggregates linked by an extracellular organic matrix. Beyond the WTSP, our data are supported by analysis of the Tara Oceans metagenomes collected in other ocean basins, showing that diazotrophs are systematically detected in mesopelagic waters when present at the surf...

Research paper thumbnail of Abundance of symbiotic and free-living diazotrophic cyanobacteria in the western tropical South Pacific during L'Atalante cruise OUTPACE in 2015

Eight different cyanobacterial diazotrophs (Trichodesmium spp., UCYN-A1, UCYN-A2, UCYN-B, UCYN-C,... more Eight different cyanobacterial diazotrophs (Trichodesmium spp., UCYN-A1, UCYN-A2, UCYN-B, UCYN-C, het-1, het-2 and het-3), and two phytoplankton hosts (UCYN-A1 and A2 hosts), were quantified by their nifH genes (18S rRNA for the hosts) in the western tropical South Pacific in spring 2015. The qPCR data was generated at 18 stations along a west to east transect from New Caledonia to Tahiti, covering oligotrophic to ultra-oligotrophic waters.

Research paper thumbnail of Diazotroph-Derived Nitrogen Assimilation Strategies Differ by Scleractinian Coral Species

Frontiers in Marine Science

Reef-building corals generally thrive in nutrient-poor tropical waters, where among other element... more Reef-building corals generally thrive in nutrient-poor tropical waters, where among other elements, nitrogen (N) availability often limits primary productivity. In addition to their close association with endosymbiotic dinoflagellates of the family Symbiodiniaceae, enabling an effective use and retention of dissolved inorganic nitrogen (DIN), scleractinian corals have developed strategies to acquire new N: (1) They can ingest N-rich sediment particles and preys (from picoplankton to macro-zooplankton) via heterotrophy, including diazotrophs [plankton fixing dinitrogen (N2) and releasing part of this nitrogen—Diazotroph-Derived N (DDN)—in seawater], a pathway called “heterotrophic nutrition on diazotrophs”; (2) Symbiotic diazotrophs located in the coral holobiont have the molecular machinery to fix N2, a pathway called “symbiotic N2 fixation”. Here we used the 15N2 isotopic labeling in a series of incubations to investigate the relative contribution of each of these DDN transfer path...

Research paper thumbnail of Fine scale sampling unveils diazotroph patchiness in the South Pacific Ocean

Diazotrophs are important contributors to reactive nitrogen availability in the ocean. Oceanograp... more Diazotrophs are important contributors to reactive nitrogen availability in the ocean. Oceanographic cruise data accumulated along decades has revealed a heterogeneous distribution of diazotroph species at regional to global scales. However, the role of dynamic fine scale structures in distributing diazotrophs is not well understood. This is due to typical insufficient spatiotemporal resolution sampling and the lack of detailed physical studies in parallel. Here we show the distribution of five groups of diazotrophs in the South Pacific at an unprecedented resolution of 7-16 km. We find a patchy distribution of diazotrophs, with each group being differently affected by parameters describing fine scale structures. The observed variability could not have been revealed with a lower resolution sampling, highlighting the need to consider fine scale physics to resolve the distribution of diazotrophs in the ocean.

Research paper thumbnail of A critical review of the 15 N 2 tracer method to measure diazotrophic production in pelagic ecosystems

Limnology and Oceanography: Methods

Research paper thumbnail of The Delayed Island Mass Effect: how islands can remotely trigger blooms in the oligotrophic ocean

Geophysical Research Letters

Research paper thumbnail of Water column nitrate+nitrite d15N measurements from R/V L'Atalante in the southwest Pacific Ocean between New Caledonia and Tahiti from February to March 2015

Biological and Chemical Oceanography Data Management Office

Research paper thumbnail of Biogeography of N 2 fixation influenced by the western boundary current intrusion in the South China Sea

Journal of Geophysical Research: Oceans

The N 2 fixation and primary production rates were measured simultaneously using 15 N 2 and 13 C ... more The N 2 fixation and primary production rates were measured simultaneously using 15 N 2 and 13 C incubation assays in the northern South China Sea influenced by the Kuroshio intrusion (KI) seasonally. The degree of KI (KI index, range from 0 to 1) was assessed by applying an isopycnal mixing model. The water column integrated N 2 fixation and primary production for stations with KI index larger than 0.5 were 463 ± 260 μmol N•m −2 •day −1 and 62 ± 19 mmol C•m −2 •day −1 , respectively, significantly higher than those for stations with KI index lower than 0.5 (50 ± 10 μmol N•m −2 •day −1 and 28 ± 10 mmol C•m −2 •day −1 , respectively). Trichodesmium was the dominant diazotroph at stations with KI index larger than 0.5, with 2 orders of magnitude higher nifH gene abundance than that at stations with KI index lower than 0.5. However, the highest N 2 fixation rates were found in waters with moderate KI index around 0.6, suggesting that frontal zone mixing might stimulate N 2 fixation. Our results demonstrated that diazotrophs (mainly Trichodesmium) were tightly associated with the KI, which modulated the biogeographic distribution of N 2 fixers. In summary, we found the transportation of Trichodesmium by KI, then, we quantified the fraction of KI and N 2 fixation rates in the northern South China Sea. The results suggested that KI generated a new biogeographic regime which could significantly influence the carbon and nitrogen cycles far away from the main stream. (SZ1914). Thanks for help from technicians Tian Li and Zou Wenbin in determination of POC and PON and their δ 13 C and δ 15 N values, who are in our Nitrogen Cycle Group at the State Key Laboratory of Marine Environmental Science (Xiamen University, China). Data sets for this paper are available in the supporting information.

Research paper thumbnail of Distributions and Abundances of Sublineages of the N2-Fixing Cyanobacterium Candidatus Atelocyanobacterium thalassa (UCYN-A) in the New Caledonian Coral Lagoon

Frontiers in Microbiology

Nitrogen (N 2) fixation is a major source of nitrogen that supports primary production in the vas... more Nitrogen (N 2) fixation is a major source of nitrogen that supports primary production in the vast oligotrophic areas of the world's oceans. The Western Tropical South Pacific has recently been identified as a hotspot for N 2 fixation. In the Noumea lagoon (New Caledonia), high abundances of the unicellular N 2-fixing cyanobacteria group A (UCYN-A), coupled with daytime N 2 fixation rates associated with the <10 µm size fraction, suggest UCYN-A may be an important diazotroph (N 2-fixer) in this region. However, little is known about the seasonal variability and diversity of UCYN-A there. To assess this, surface waters from a 12 km transect from the mouth of the Dumbea River to the Dumbea Pass were sampled monthly between July 2012 and March 2014. UCYN-A abundances for two of the defined sublineages, UCYN-A1 and UCYN-A2, were quantified using qPCR targeting the nifH gene, and the nifH-based diversity of UCYN-A was characterized by identifying oligotypes, alternative taxonomic units defined by nucleotide positions with high variability. UCYN-A abundances were dominated by the UCYN-A1 sublineage, peaked in September and October and could be predicted by a suite of nine environmental parameters. At the sublineage level, UCYN-A1 abundances could be predicted based on lower temperatures (<23 • C), nitrate concentrations, precipitation, wind speed, while UCYN-A2 abundances could be predicted based on silica, and chlorophyll a concentrations, wind direction, precipitation, and wind speed. Using UCYN-A nifH oligotyping, similar environmental variables explained the relative abundances of sublineages and their associated oligotypes, with the notable exception of the UCYN-A2 oligotype (oligo43) which had relative abundance patterns distinct from the dominant UCYN-A2 oligotype (oligo3). The results support an emerging pattern that UCYN-A is comprised of a diverse group of strains, with sublineages that may have different ecological niches. By identifying environmental factors that influence the composition and abundance of UCYN-A sublineages, this study helps to explain global UCYN-A abundance patterns, and is important for understanding the significance of N 2 fixation at local and global scales.

Research paper thumbnail of Transfer of diazotroph-derived nitrogen to the planktonic food web across gradients of N<sub>2</sub> fixation activity and diversity in the western tropical South Pacific Ocean

Biogeosciences

Biological dinitrogen (N 2) fixation provides the major source of new nitrogen (N) to the open oc... more Biological dinitrogen (N 2) fixation provides the major source of new nitrogen (N) to the open ocean, contributing more than atmospheric deposition and riverine inputs to the N supply. Yet the fate of the diazotrophderived N (DDN) in the planktonic food web is poorly understood. The main goals of this study were (i) to quantify how much of DDN is released to the dissolved pool during N 2 fixation and how much is transferred to bacteria, phytoplankton and zooplankton, and (ii) to compare the DDN release and transfer efficiencies under contrasting N 2 fixation activity and diversity in the oligotrophic waters of the western tropical South Pacific (WTSP) Ocean. We used nanometre-scale secondary ion mass spectrometry (nanoSIMS) coupled with 15 N 2 isotopic labelling and flow cytometry cell sorting to track the DDN transfer to plankton, in regions where the diazotroph community was dominated by either Trichodesmium or by UCYN-B. After 48 h, ∼ 20-40 % of the N 2 fixed during the experiment was released to the dissolved pool when Trichodesmium dominated, while the DDN release was not quantifiable when UCYN-B dominated; ∼ 7-15 % of the total fixed N (net N 2 fixation + release) was transferred to non-diazotrophic plankton within 48 h, with higher transfer efficiencies (15 ± 3 %) when UCYN-B dominated as compared to when Trichodesmium dominated (9 ± 3 %). The pico-cyanobacteria Synechococcus and Prochlorococcus were the primary beneficiaries of the DDN transferred (∼ 65-70 %), followed by heterotrophic bacteria (∼ 23-34 %). The DDN transfer in bacteria was higher (34 ± 7 %) in the UCYN-B-dominating experiment compared to the Trichodesmium-dominating experiments (24 ± 5 %). Regarding higher trophic levels, the DDN transfer to the dominant zooplankton species was less efficient when the diazotroph community was dominated by Trichodesmium (∼ 5-9 % of the DDN transfer) than when it was dominated by UCYN-B (∼ 28 ± 13 % of the DDN transfer). To our knowledge, this study provides the first quantification of DDN release and transfer to phytoplankton, bacteria and zooplankton communities in open ocean waters. It reveals that despite UCYN-B fix N 2 at lower rates compared to Trichodesmium in the WTSP, the DDN from UCYN-B is much more available and efficiently transferred to the planktonic food web than the DDN originating from Trichodesmium.

Research paper thumbnail of Distribution and rates of nitrogen fixation in the western tropical South Pacific Ocean constrained by nitrogen isotope budgets

Biogeosciences

Constraining the rates and spatial distribution of dinitrogen (N 2) fixation fluxes to the ocean ... more Constraining the rates and spatial distribution of dinitrogen (N 2) fixation fluxes to the ocean informs our understanding of the environmental sensitivities of N 2 fixation as well as the timescale over which the fluxes of nitrogen (N) to and from the ocean may respond to each other. Here we quantify rates of N 2 fixation as well as its contribution to export production along a zonal transect in the western tropical South Pacific (WTSP) Ocean using N isotope ("δ 15 N") budgets. Comparing measurements of water column nitrate + nitrite δ 15 N with the δ 15 N of sinking particulate N at a western, central, and eastern station, these δ 15 N budgets indicate high, modest, and low rates of N 2 fixation at the respective stations. The results also imply that N 2 fixation supports exceptionally high, i.e. ≥ 50 %, of export production at the western and central stations, which are also proximal to the largest iron sources. These geochemically based rates of N 2 fixation are equal to or greater than those previously reported in the tropical North Atlantic, indicating that the WTSP Ocean has the capacity to support globally significant rates of N 2 fixation, which may compensate for N removal in the oxygen-deficient zones of the eastern tropical Pacific.

Research paper thumbnail of In-depth characterization of diazotroph activity across the western tropical South Pacific hotspot of N<sub>2</sub> fixation (OUTPACE cruise)

Biogeosciences

Here we report N 2 fixation rates from a ∼ 4000 km transect in the western and central tropical S... more Here we report N 2 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 ultraoligotrophy in the South Pacific Gyre (GY) waters. N 2 fixation was detected at all 17 sampled stations with an average depth-integrated rate of 631 ± 286 µmol N m −2 d −1 (range 196-1153 µmol N m −2 d −1) in MA waters and of 85 ± 79 µmol N m −2 d −1 (range 18-172 µmol N m −2 d −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 > 10 5 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 N 2 fixation in MA waters, accounting for 47.1-83.8 % of bulk N 2 fixation. The most plausible environmental factors explaining such exceptionally high rates of N 2 fixation in MA waters are discussed in detail, emphasizing the role of macro-and micro-nutrient (e.g., iron) availability, seawater temperature and currents.

Research paper thumbnail of N<sub>2</sub> fixation as a dominant new N source in the western tropical South Pacific Ocean (OUTPACE cruise)

Research paper thumbnail of Excess nitrogen as a marker of intense dinitrogen fixation in the Western Tropical South Pacific Ocean: impact on the thermocline waters of the South Pacific

Biogeosciences Discussions

As part of the Oligotrophy to UlTra-oligotrophy PACific Experiment cruise, which took place in th... more As part of the Oligotrophy to UlTra-oligotrophy PACific Experiment cruise, which took place in the Western 15 Tropical South Pacific during the austral summer (March-April 2015), we present data on nitrate, phosphate and on particulate and dissolved organic matter. The stoichiometric nitrogen-to-phosphorus ratios of the inorganic and organic material and the tracer N* are described. N* allows to trace changes in the proportion of fixed nitrogen due to diazotrophy and/or denitrification. Our results showed that the Melanesian archipelago waters between 160° E and 170° W are characterized by a deficit of nitrate and phosphate in the productive layer, significant dinitrogen fixation rates and an excess of particulate organic nitrogen 20 compared to the canonical ratio of Redfield. A positive N* anomaly was observed in the productive layer reflecting the combined effect of phosphate uptake by diazotrophic organisms and remineralization of excess particulate organic nitrogen. The South Pacific Gyre waters between 170° W and 160° W were depleted in nitrate but rich in phosphate. Surface waters exhibited very low dinitrogen fixation rates, an absence of excess particulate organic nitrogen and a N* signal close to zero. The higher iron availability coupled with an absence of nitrate in the suface water of the Melanesian archipelago could 25 stimulate the diazotrophic activity, which in turn will introduce excess nitrogen, deplete the surface waters in phosphate and be the explanation for the positive N* anomaly in the Melanesian archipelago waters. In the thermocline waters, the N* tracer revealed its full complexity, with notably the cumulative effect of the remineralization of particulate organic nitrogen and the effects of the mixing of water masses. At the global ocean scale, calculation of N* signal from the new Global Ocean Data Analysis Project version 2 database showed a strong spatial decoupling between the thermocline waters of the Eastern Tropical 30 South Pacific and those of the Western Tropical South Pacific. A strongly positive N* anomaly was observed in the thermocline waters of the Western Tropical South Pacific in the Coral/Tasman Seas and in the southern part of the subtropical gyre between latitude 23° S and 32° S. A strong negative N* signal was observed in the waters of the Eestern Tropical South Pacific between latitude 5°S and 20°S-23°S. We hypothesise that the nitrogen excess observed in the thermocline waters of the Western Tropical South Pacific is transported eastward and then northward by the circulation of the South Pacific subtropical gyre and 35 could influence positively the thermocline waters of the South Pacific being thus at the origin of the westward increase of the strongly negative N* signal transported by the South Equatorial Current. 1 Introduction It is commonly accepted that net biological activity is supported by the supply of new nitrogen into the surface productive layer (Dugdale and Goering, 1967; Capone et al., 2005). At the global ocean scale, Redfield et al. (1963) reported similarity 40

Research paper thumbnail of Iron from a submarine source impacts the productive layer of the Western Tropical South Pacific (WTSP)

Scientific reports, Jan 13, 2018

In the Western Tropical South Pacific, patches of high chlorophyll concentrations linked to the o... more In the Western Tropical South Pacific, patches of high chlorophyll concentrations linked to the occurrence of N-fixing organisms are found in the vicinity of volcanic islands. The survival of these organisms relies on a high bioavailable iron supply whose origin and fluxes remain unknown. Here, we measured high dissolved iron (DFe) concentrations (up to 66 nM) in the euphotic layer, extending zonally over 10 degrees longitude (174 E-175 W) at ∼20°S latitude. DFe atmospheric fluxes were at the lower end of reported values of the remote ocean and could not explain the high DFe concentrations measured in the water column in the vicinity of Tonga. We argue that the high DFe concentrations may be sustained by a submarine source, also characterized by freshwater input and recorded as salinity anomalies by Argo float in situ measurements and atlas data. The observed negative salinity anomalies are reproduced by simulations from a general ocean circulation model. Submarine iron sources reac...

Research paper thumbnail of Diazotrophs are overlooked contributors to carbon and nitrogen export to the deep ocean

The ISME Journal

Diazotrophs are widespread microorganisms that alleviate nitrogen limitation in 60% of our oceans... more Diazotrophs are widespread microorganisms that alleviate nitrogen limitation in 60% of our oceans, thereby regulating marine productivity. Yet, the group-specific contribution of diazotrophs to organic matter export has not been quantified, which so far has impeded an accurate assessment of their impact on the biological carbon pump. Here, we examine the fate of five groups of globally-distributed diazotrophs by using an original combination of mesopelagic particle sampling devices across the subtropical South Pacific Ocean. We demonstrate that cyanobacterial and non-cyanobacterial diazotrophs are exported down to 1000 m depth. Surprisingly, group-specific export turnover rates point to a more efficient export of small unicellular cyanobacterial diazotrophs (UCYN) relative to the larger and filamentous Trichodesmium. Phycoerythrin-containing UCYN-B and UCYN-C-like cells were recurrently found embedded in large (>50 µm) organic aggregates or organized into clusters of tens to hund...

Research paper thumbnail of Dissolved organic matter stimulates N₂ fixation and nifH gene expression in Trichodesmium

FEMS Microbiology Letters, Apr 6, 2020

Mixotrophy, the combination of heterotrophic and autotrophic nutrition modes, is emerging as the ... more Mixotrophy, the combination of heterotrophic and autotrophic nutrition modes, is emerging as the rule rather than the exception in marine photosynthetic plankton. Trichodesmium, a prominent diazotroph ubiquitous in the (sub)tropical oceans, is generally considered to obtain energy via autotrophy. While the ability of Trichodesmium to use dissolved organic phosphorus when deprived of inorganic phosphorus sources is well known, the extent to which this important cyanobacterium may benefit from other dissolved organic matter (DOM) sources is unknown. Here we provide evidence of carbon-, nitrogen- and phosphorus-rich DOM molecules enhancing N₂ fixation rates and nifH gene expression in natural Trichodesmium colonies collected at two stations in the western tropical South Pacific. Sampling at a third station located in the oligotrophic South Pacific Gyre revealed no Trichodesmium but showed presence of UCYN-B, although no nifH expression was detected. Our results suggest that Trichodesmi...

Research paper thumbnail of Diazotroph community and activity in the Southern Indian Ocean

Research paper thumbnail of Insights into nitrogen fixation below the euphotic zone: trials in an oligotrophic marginal sea and global compilation

Nitrogen (N2) fixation, the energetically expensive conversion of N2 to ammonia, plays an importa... more Nitrogen (N2) fixation, the energetically expensive conversion of N2 to ammonia, plays an important role in balancing the global nitrogen budget. Defying historic paradigms, recent studies have detected non-cyanobacterial N2 fixation in deep, dark oceanic waters. Even low volumetric rates can be significant considering the large volume of these waters. However, measuring aphotic N2 fixation is an analytical challenge due to the low particulate nitrogen (PN) concentrations. Here, we investigated N2 fixation rates in aphotic waters in the South China Sea (SCS). To increase the sensitivity of N2 fixation rate measurements, we applied a novel approach requiring only 0.28 μg N for measuring the isotopic composition of particulate nitrogen. We conducted parallel 15 N2-enriched incubations in ambient seawater, seawater amended with amino acids and poisoned (HgCl2) controls, along with incubations that received no tracer additions to distinguish biological N2 fixation. Experimental treatments differed significantly from our two types of controls, those receiving no additions and killed controls. Amino acid additions masked N2 fixation signals due to the uptake of added 14 Namino acid. Results show that the maximum dark N2 fixation rates (1.28 ± 0.85 nmol N L-1 d-1) occurred within upper 200 m, while rates below 200 m were mostly lower than 0.1 nmol N L-1 d-1. Nevertheless, N2 fixation rates between 200 and 1000 m accounted for 39 ± 32 % of depth-integrated dark N2 fixation rates in the upper 1000 m, which is comparable to the areal nitrogen inputs via atmospheric deposition. Globally, we found that aphotic N2 fixation studies conducted in oxygenated environments yielded rates similar to those from the SCS (< 1 nmol N L-1 d-1), regardless of methods, while higher rates were occasionally observed in low-oxygen (< 62 µM) regions. Regression analysis suggests that particulate nitrogen concentrations could be a predictive proxy for detectable aphotic N2 fixation in the SCS and eastern tropical south Pacific.

Research paper thumbnail of Seasonal Shifts in Diazotrophs Players: Patterns Observed Over a Two-Year Time Series in the New Caledonian Lagoon (Western Tropical South Pacific Ocean)

Coastal and open ocean regions of the Western Tropical South Pacific ocean have been identified a... more Coastal and open ocean regions of the Western Tropical South Pacific ocean have been identified as a hotspot of N2 fixation. However, the environmental factors driving the temporal variability of abundance, composition, and activity of diazotrophs are still poorly understood, especially during the winter season. To address this, we quantified N2 fixation rates and the abundance of seven diazotroph phylotypes (UCYN-A1 symbiosis, UCYN-B, UCYN-C, Trichodesmium, Het-1, Het-2, and Het-3) on a monthly basis during two full years (2012 to 2014) at four stations along a coast to open ocean transect in the New Caledonian lagoon. The total nifH gene concentration (sum of all nifH gene copies) clearly decreased from the barrier reef to the shore. Apart from UCYN-B, which peaked at very high abundances (106–108 nifH gene copies L–1) at two occasions at the coastal station, the UCYN-A1 symbiosis was the most abundant group at all stations, accounting for 79% of the total nifH gene copy counts al...

Research paper thumbnail of Massive export of diazotrophs across the South Pacific tropical Ocean

bioRxiv, 2021

Diazotrophs are widespread microorganisms that alleviate nitrogen limitation in 60% of our oceans... more Diazotrophs are widespread microorganisms that alleviate nitrogen limitation in 60% of our oceans, regulating marine productivity. Yet, their contribution to organic matter export has not been quantified, making an assessment of their impact on the biological carbon pump impossible. Here, we demonstrate that cyanobacterial and non-cyanobacterial diazotrophs are massively exported down to 1000 m-depth in the western subtropical South Pacific Ocean (WTSP), accounting for up to 52-100% of the total particulate nitrogen export fluxes. We further demonstrate that small size unicellular diazotrophs (UCYN, 1-8 µm) are exported more efficiently than filamentous diazotrophs (>100-1000 µm) under the form of large (>50 µm) aggregates linked by an extracellular organic matrix. Beyond the WTSP, our data are supported by analysis of the Tara Oceans metagenomes collected in other ocean basins, showing that diazotrophs are systematically detected in mesopelagic waters when present at the surf...

Research paper thumbnail of Abundance of symbiotic and free-living diazotrophic cyanobacteria in the western tropical South Pacific during L'Atalante cruise OUTPACE in 2015

Eight different cyanobacterial diazotrophs (Trichodesmium spp., UCYN-A1, UCYN-A2, UCYN-B, UCYN-C,... more Eight different cyanobacterial diazotrophs (Trichodesmium spp., UCYN-A1, UCYN-A2, UCYN-B, UCYN-C, het-1, het-2 and het-3), and two phytoplankton hosts (UCYN-A1 and A2 hosts), were quantified by their nifH genes (18S rRNA for the hosts) in the western tropical South Pacific in spring 2015. The qPCR data was generated at 18 stations along a west to east transect from New Caledonia to Tahiti, covering oligotrophic to ultra-oligotrophic waters.

Research paper thumbnail of Diazotroph-Derived Nitrogen Assimilation Strategies Differ by Scleractinian Coral Species

Frontiers in Marine Science

Reef-building corals generally thrive in nutrient-poor tropical waters, where among other element... more Reef-building corals generally thrive in nutrient-poor tropical waters, where among other elements, nitrogen (N) availability often limits primary productivity. In addition to their close association with endosymbiotic dinoflagellates of the family Symbiodiniaceae, enabling an effective use and retention of dissolved inorganic nitrogen (DIN), scleractinian corals have developed strategies to acquire new N: (1) They can ingest N-rich sediment particles and preys (from picoplankton to macro-zooplankton) via heterotrophy, including diazotrophs [plankton fixing dinitrogen (N2) and releasing part of this nitrogen—Diazotroph-Derived N (DDN)—in seawater], a pathway called “heterotrophic nutrition on diazotrophs”; (2) Symbiotic diazotrophs located in the coral holobiont have the molecular machinery to fix N2, a pathway called “symbiotic N2 fixation”. Here we used the 15N2 isotopic labeling in a series of incubations to investigate the relative contribution of each of these DDN transfer path...

Research paper thumbnail of Fine scale sampling unveils diazotroph patchiness in the South Pacific Ocean

Diazotrophs are important contributors to reactive nitrogen availability in the ocean. Oceanograp... more Diazotrophs are important contributors to reactive nitrogen availability in the ocean. Oceanographic cruise data accumulated along decades has revealed a heterogeneous distribution of diazotroph species at regional to global scales. However, the role of dynamic fine scale structures in distributing diazotrophs is not well understood. This is due to typical insufficient spatiotemporal resolution sampling and the lack of detailed physical studies in parallel. Here we show the distribution of five groups of diazotrophs in the South Pacific at an unprecedented resolution of 7-16 km. We find a patchy distribution of diazotrophs, with each group being differently affected by parameters describing fine scale structures. The observed variability could not have been revealed with a lower resolution sampling, highlighting the need to consider fine scale physics to resolve the distribution of diazotrophs in the ocean.

Research paper thumbnail of A critical review of the 15 N 2 tracer method to measure diazotrophic production in pelagic ecosystems

Limnology and Oceanography: Methods

Research paper thumbnail of The Delayed Island Mass Effect: how islands can remotely trigger blooms in the oligotrophic ocean

Geophysical Research Letters

Research paper thumbnail of Water column nitrate+nitrite d15N measurements from R/V L'Atalante in the southwest Pacific Ocean between New Caledonia and Tahiti from February to March 2015

Biological and Chemical Oceanography Data Management Office

Research paper thumbnail of Biogeography of N 2 fixation influenced by the western boundary current intrusion in the South China Sea

Journal of Geophysical Research: Oceans

The N 2 fixation and primary production rates were measured simultaneously using 15 N 2 and 13 C ... more The N 2 fixation and primary production rates were measured simultaneously using 15 N 2 and 13 C incubation assays in the northern South China Sea influenced by the Kuroshio intrusion (KI) seasonally. The degree of KI (KI index, range from 0 to 1) was assessed by applying an isopycnal mixing model. The water column integrated N 2 fixation and primary production for stations with KI index larger than 0.5 were 463 ± 260 μmol N•m −2 •day −1 and 62 ± 19 mmol C•m −2 •day −1 , respectively, significantly higher than those for stations with KI index lower than 0.5 (50 ± 10 μmol N•m −2 •day −1 and 28 ± 10 mmol C•m −2 •day −1 , respectively). Trichodesmium was the dominant diazotroph at stations with KI index larger than 0.5, with 2 orders of magnitude higher nifH gene abundance than that at stations with KI index lower than 0.5. However, the highest N 2 fixation rates were found in waters with moderate KI index around 0.6, suggesting that frontal zone mixing might stimulate N 2 fixation. Our results demonstrated that diazotrophs (mainly Trichodesmium) were tightly associated with the KI, which modulated the biogeographic distribution of N 2 fixers. In summary, we found the transportation of Trichodesmium by KI, then, we quantified the fraction of KI and N 2 fixation rates in the northern South China Sea. The results suggested that KI generated a new biogeographic regime which could significantly influence the carbon and nitrogen cycles far away from the main stream. (SZ1914). Thanks for help from technicians Tian Li and Zou Wenbin in determination of POC and PON and their δ 13 C and δ 15 N values, who are in our Nitrogen Cycle Group at the State Key Laboratory of Marine Environmental Science (Xiamen University, China). Data sets for this paper are available in the supporting information.

Research paper thumbnail of Distributions and Abundances of Sublineages of the N2-Fixing Cyanobacterium Candidatus Atelocyanobacterium thalassa (UCYN-A) in the New Caledonian Coral Lagoon

Frontiers in Microbiology

Nitrogen (N 2) fixation is a major source of nitrogen that supports primary production in the vas... more Nitrogen (N 2) fixation is a major source of nitrogen that supports primary production in the vast oligotrophic areas of the world's oceans. The Western Tropical South Pacific has recently been identified as a hotspot for N 2 fixation. In the Noumea lagoon (New Caledonia), high abundances of the unicellular N 2-fixing cyanobacteria group A (UCYN-A), coupled with daytime N 2 fixation rates associated with the <10 µm size fraction, suggest UCYN-A may be an important diazotroph (N 2-fixer) in this region. However, little is known about the seasonal variability and diversity of UCYN-A there. To assess this, surface waters from a 12 km transect from the mouth of the Dumbea River to the Dumbea Pass were sampled monthly between July 2012 and March 2014. UCYN-A abundances for two of the defined sublineages, UCYN-A1 and UCYN-A2, were quantified using qPCR targeting the nifH gene, and the nifH-based diversity of UCYN-A was characterized by identifying oligotypes, alternative taxonomic units defined by nucleotide positions with high variability. UCYN-A abundances were dominated by the UCYN-A1 sublineage, peaked in September and October and could be predicted by a suite of nine environmental parameters. At the sublineage level, UCYN-A1 abundances could be predicted based on lower temperatures (<23 • C), nitrate concentrations, precipitation, wind speed, while UCYN-A2 abundances could be predicted based on silica, and chlorophyll a concentrations, wind direction, precipitation, and wind speed. Using UCYN-A nifH oligotyping, similar environmental variables explained the relative abundances of sublineages and their associated oligotypes, with the notable exception of the UCYN-A2 oligotype (oligo43) which had relative abundance patterns distinct from the dominant UCYN-A2 oligotype (oligo3). The results support an emerging pattern that UCYN-A is comprised of a diverse group of strains, with sublineages that may have different ecological niches. By identifying environmental factors that influence the composition and abundance of UCYN-A sublineages, this study helps to explain global UCYN-A abundance patterns, and is important for understanding the significance of N 2 fixation at local and global scales.

Research paper thumbnail of Transfer of diazotroph-derived nitrogen to the planktonic food web across gradients of N<sub>2</sub> fixation activity and diversity in the western tropical South Pacific Ocean

Biogeosciences

Biological dinitrogen (N 2) fixation provides the major source of new nitrogen (N) to the open oc... more Biological dinitrogen (N 2) fixation provides the major source of new nitrogen (N) to the open ocean, contributing more than atmospheric deposition and riverine inputs to the N supply. Yet the fate of the diazotrophderived N (DDN) in the planktonic food web is poorly understood. The main goals of this study were (i) to quantify how much of DDN is released to the dissolved pool during N 2 fixation and how much is transferred to bacteria, phytoplankton and zooplankton, and (ii) to compare the DDN release and transfer efficiencies under contrasting N 2 fixation activity and diversity in the oligotrophic waters of the western tropical South Pacific (WTSP) Ocean. We used nanometre-scale secondary ion mass spectrometry (nanoSIMS) coupled with 15 N 2 isotopic labelling and flow cytometry cell sorting to track the DDN transfer to plankton, in regions where the diazotroph community was dominated by either Trichodesmium or by UCYN-B. After 48 h, ∼ 20-40 % of the N 2 fixed during the experiment was released to the dissolved pool when Trichodesmium dominated, while the DDN release was not quantifiable when UCYN-B dominated; ∼ 7-15 % of the total fixed N (net N 2 fixation + release) was transferred to non-diazotrophic plankton within 48 h, with higher transfer efficiencies (15 ± 3 %) when UCYN-B dominated as compared to when Trichodesmium dominated (9 ± 3 %). The pico-cyanobacteria Synechococcus and Prochlorococcus were the primary beneficiaries of the DDN transferred (∼ 65-70 %), followed by heterotrophic bacteria (∼ 23-34 %). The DDN transfer in bacteria was higher (34 ± 7 %) in the UCYN-B-dominating experiment compared to the Trichodesmium-dominating experiments (24 ± 5 %). Regarding higher trophic levels, the DDN transfer to the dominant zooplankton species was less efficient when the diazotroph community was dominated by Trichodesmium (∼ 5-9 % of the DDN transfer) than when it was dominated by UCYN-B (∼ 28 ± 13 % of the DDN transfer). To our knowledge, this study provides the first quantification of DDN release and transfer to phytoplankton, bacteria and zooplankton communities in open ocean waters. It reveals that despite UCYN-B fix N 2 at lower rates compared to Trichodesmium in the WTSP, the DDN from UCYN-B is much more available and efficiently transferred to the planktonic food web than the DDN originating from Trichodesmium.

Research paper thumbnail of Distribution and rates of nitrogen fixation in the western tropical South Pacific Ocean constrained by nitrogen isotope budgets

Biogeosciences

Constraining the rates and spatial distribution of dinitrogen (N 2) fixation fluxes to the ocean ... more Constraining the rates and spatial distribution of dinitrogen (N 2) fixation fluxes to the ocean informs our understanding of the environmental sensitivities of N 2 fixation as well as the timescale over which the fluxes of nitrogen (N) to and from the ocean may respond to each other. Here we quantify rates of N 2 fixation as well as its contribution to export production along a zonal transect in the western tropical South Pacific (WTSP) Ocean using N isotope ("δ 15 N") budgets. Comparing measurements of water column nitrate + nitrite δ 15 N with the δ 15 N of sinking particulate N at a western, central, and eastern station, these δ 15 N budgets indicate high, modest, and low rates of N 2 fixation at the respective stations. The results also imply that N 2 fixation supports exceptionally high, i.e. ≥ 50 %, of export production at the western and central stations, which are also proximal to the largest iron sources. These geochemically based rates of N 2 fixation are equal to or greater than those previously reported in the tropical North Atlantic, indicating that the WTSP Ocean has the capacity to support globally significant rates of N 2 fixation, which may compensate for N removal in the oxygen-deficient zones of the eastern tropical Pacific.

Research paper thumbnail of In-depth characterization of diazotroph activity across the western tropical South Pacific hotspot of N<sub>2</sub> fixation (OUTPACE cruise)

Biogeosciences

Here we report N 2 fixation rates from a ∼ 4000 km transect in the western and central tropical S... more Here we report N 2 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 ultraoligotrophy in the South Pacific Gyre (GY) waters. N 2 fixation was detected at all 17 sampled stations with an average depth-integrated rate of 631 ± 286 µmol N m −2 d −1 (range 196-1153 µmol N m −2 d −1) in MA waters and of 85 ± 79 µmol N m −2 d −1 (range 18-172 µmol N m −2 d −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 > 10 5 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 N 2 fixation in MA waters, accounting for 47.1-83.8 % of bulk N 2 fixation. The most plausible environmental factors explaining such exceptionally high rates of N 2 fixation in MA waters are discussed in detail, emphasizing the role of macro-and micro-nutrient (e.g., iron) availability, seawater temperature and currents.

Research paper thumbnail of N<sub>2</sub> fixation as a dominant new N source in the western tropical South Pacific Ocean (OUTPACE cruise)

Research paper thumbnail of Excess nitrogen as a marker of intense dinitrogen fixation in the Western Tropical South Pacific Ocean: impact on the thermocline waters of the South Pacific

Biogeosciences Discussions

As part of the Oligotrophy to UlTra-oligotrophy PACific Experiment cruise, which took place in th... more As part of the Oligotrophy to UlTra-oligotrophy PACific Experiment cruise, which took place in the Western 15 Tropical South Pacific during the austral summer (March-April 2015), we present data on nitrate, phosphate and on particulate and dissolved organic matter. The stoichiometric nitrogen-to-phosphorus ratios of the inorganic and organic material and the tracer N* are described. N* allows to trace changes in the proportion of fixed nitrogen due to diazotrophy and/or denitrification. Our results showed that the Melanesian archipelago waters between 160° E and 170° W are characterized by a deficit of nitrate and phosphate in the productive layer, significant dinitrogen fixation rates and an excess of particulate organic nitrogen 20 compared to the canonical ratio of Redfield. A positive N* anomaly was observed in the productive layer reflecting the combined effect of phosphate uptake by diazotrophic organisms and remineralization of excess particulate organic nitrogen. The South Pacific Gyre waters between 170° W and 160° W were depleted in nitrate but rich in phosphate. Surface waters exhibited very low dinitrogen fixation rates, an absence of excess particulate organic nitrogen and a N* signal close to zero. The higher iron availability coupled with an absence of nitrate in the suface water of the Melanesian archipelago could 25 stimulate the diazotrophic activity, which in turn will introduce excess nitrogen, deplete the surface waters in phosphate and be the explanation for the positive N* anomaly in the Melanesian archipelago waters. In the thermocline waters, the N* tracer revealed its full complexity, with notably the cumulative effect of the remineralization of particulate organic nitrogen and the effects of the mixing of water masses. At the global ocean scale, calculation of N* signal from the new Global Ocean Data Analysis Project version 2 database showed a strong spatial decoupling between the thermocline waters of the Eastern Tropical 30 South Pacific and those of the Western Tropical South Pacific. A strongly positive N* anomaly was observed in the thermocline waters of the Western Tropical South Pacific in the Coral/Tasman Seas and in the southern part of the subtropical gyre between latitude 23° S and 32° S. A strong negative N* signal was observed in the waters of the Eestern Tropical South Pacific between latitude 5°S and 20°S-23°S. We hypothesise that the nitrogen excess observed in the thermocline waters of the Western Tropical South Pacific is transported eastward and then northward by the circulation of the South Pacific subtropical gyre and 35 could influence positively the thermocline waters of the South Pacific being thus at the origin of the westward increase of the strongly negative N* signal transported by the South Equatorial Current. 1 Introduction It is commonly accepted that net biological activity is supported by the supply of new nitrogen into the surface productive layer (Dugdale and Goering, 1967; Capone et al., 2005). At the global ocean scale, Redfield et al. (1963) reported similarity 40

Research paper thumbnail of Iron from a submarine source impacts the productive layer of the Western Tropical South Pacific (WTSP)

Scientific reports, Jan 13, 2018

In the Western Tropical South Pacific, patches of high chlorophyll concentrations linked to the o... more In the Western Tropical South Pacific, patches of high chlorophyll concentrations linked to the occurrence of N-fixing organisms are found in the vicinity of volcanic islands. The survival of these organisms relies on a high bioavailable iron supply whose origin and fluxes remain unknown. Here, we measured high dissolved iron (DFe) concentrations (up to 66 nM) in the euphotic layer, extending zonally over 10 degrees longitude (174 E-175 W) at ∼20°S latitude. DFe atmospheric fluxes were at the lower end of reported values of the remote ocean and could not explain the high DFe concentrations measured in the water column in the vicinity of Tonga. We argue that the high DFe concentrations may be sustained by a submarine source, also characterized by freshwater input and recorded as salinity anomalies by Argo float in situ measurements and atlas data. The observed negative salinity anomalies are reproduced by simulations from a general ocean circulation model. Submarine iron sources reac...