Abstract
The unicellular diazotrophic cyanobacterium Crocosphaera contributes significantly to fixed nitrogen inputs in the oligotrophic ocean. In the western tropical South Pacific Ocean (WTSP), ...these diazotrophs abound thanks to the phosphorus-rich waters provided by the South Equatorial Current, and iron provided aeolian and subsurface volcanic activity. East of the WTSP, the South Pacific Gyre (SPG) harbors the most oligotrophic and transparent waters of the world's oceans, where only heterotrophic diazotrophs have been reported before. Here, in the SPG, we detected unexpected accumulation of Crocosphaera at 50 m with peak abundances of 5.26 × 105 nifH gene copies l–1. The abundance of Crocosphaera at 50 m was in the same order of magnitude as those detected westwards in the WTSP and represented 100% of volumetric N2 fixation rates. This accumulation at 50 m was likely due to a deeper penetration of UV light in the clear waters of the SPG being detrimental for Crocosphaera growth and N2 fixation activity. Nutrient and trace metal addition experiments did not induce any significant changes in N2 fixation or Crocosphaera abundance, indicating that this population was not limited by the resources tested and could develop in high numbers despite the oligotrophic conditions. Our findings indicate that the distribution of Crocosphaera can extend into subtropical gyres and further understanding of their controlling factors is needed.
We find diazotrophically active Crocosphaera in the clearest waters of the world's oceans.
Allochthonous and autochthonous dissolved organic matter (DOM) and nutrient availability (nitrogen N, phosphorus P) are expected to increase in lakes as a consequence of climate change. These ...increases can alter the planktonic food web, especially in oligotrophic systems.
This study addresses the consequences of DOM and nutrient increase on heterotrophic bacterioplankton (Hbact) and phytoplankton in high‐altitude lakes. A planktonic community from a high‐altitude lake was incubated for 10 days and laboratory microcosms were subjected to a full factorial design 4 × 2 × 2 of three factors: carbon (C‐control, glucose, algal lysate, soil extract), inorganic nutrients (no added nutrients, addition of N and P) and light (light:dark cycle, dark).
Hbact was co‐limited by organic C and inorganic nutrients, resulting in lower biomass and production with glucose or inorganic nutrients added alone than with the two sources added in combination. Algal‐derived DOM was more labile, more consumed, and resulted in higher bacterial production, while soil‐derived DOM was less labile and less consumed. Phytoplankton was strongly limited by inorganic nutrients. DOM additions, via the interactions with Hbact, increased phytoplankton biomass and modified the community composition. Mixotrophs increased with C under light or nutrient limitation, pointing them as major factors in controlling mixotrophy in high‐altitude lakes. Soil‐derived DOM led to higher algal biomass, higher proportion of mixotrophs, and more taxa adapted to nutrient‐enriched conditions.
This study reveals a shift in planktonic interactions with changes in DOM quality and quantity. Under the projected climate change, we expect an increase in heterotrophy and a modification of trophic interactions with important repercussions on the C cycle in high‐altitude lakes.
ABSTRACT
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) resources 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 Trichodesmium behaves mixotrophically in response to certain environmental conditions, providing them with metabolic plasticity and adding up to the view that mixotrophy is widespread among marine microbes.
Trichodesmiumis generally considered an autotroph. This work shows an enhancement in N2 fixation and nifHgene expression in Trichodesmium as a response to dissolved organic matter compounds, indicating a mixotrophic potential.
In the marine environment, transparent exopolymeric particles (TEP) produced from abiotic and biotic sources link the particulate and dissolved carbon pools and are essential vectors enhancing ...vertical carbon flux. We characterized spatial and temporal dynamics of TEP during the VAHINE experiment that investigated the fate of diazotroph-derived nitrogen and carbon in three replicate dissolved inorganic phosphorus (DIP)-fertilized 50 m3 enclosures in the oligotrophic New Caledonian lagoon. During the 23 days of the experiment, we did not observe any depth-dependent changes in TEP concentrations in the three sampled depths (1, 6, 12 m). TEP carbon (TEP-C) content averaged 28.9 ± 9.3 and 27.0 ± 7.2 % of total organic carbon (TOC) in the mesocosms and surrounding lagoon respectively and was strongly and positively coupled with TOC during P2 (i.e., days 15–23). TEP concentrations in the mesocosms declined for the first 9 days after DIP fertilization (P1 = days 5–14) and then gradually increased during the second phase. Temporal changes in TEP concentrations paralleled the growth and mortality rates of the diatom–diazotroph association of Rhizosolenia and Richelia that predominated the diazotroph community during P1. By P2, increasing total primary and heterotrophic bacterial production consumed the supplemented P and reduced availability of DIP. For this period, TEP concentrations were negatively correlated with DIP availability and turnover time of DIP (TDIP), while positively associated with enhanced alkaline phosphatase activity (APA) that occurs when the microbial populations are P stressed. During P2, increasing bacterial production (BP) was positively correlated with higher TEP concentrations, which were also coupled with the increased growth rates and aggregation of the unicellular cyanobacterial Group C (UCYN-C) diazotrophs that bloomed during this period. We conclude that the composite processes responsible for the formation and breakdown of TEP yielded a relatively stable TEP pool available as both a carbon source and facilitating aggregation and flux throughout the experiment. TEP were probably mostly influenced by abiotic physical processes during P1, while biological activity (BP, diazotrophic growth and aggregation, export production) mainly impacted TEP concentrations during P2 when DIP availability was limited.
Summary
Cyanobacteria are major contributors to ocean biogeochemical cycling. However, mixotrophic metabolism and the relative importance of inorganic and organic carbon assimilation within the most ...abundant cyanobacteria are still poorly understood. We explore the ability of Prochlorococcus and Synechococcus to assimilate organic molecules with variable C:N:P composition and its modulation by light availability and photosynthetic impairment. We used a combination of radiolabelled molecules incubations with flow cytometry cell sorting to separate picoplankton groups from the western tropical South Pacific Ocean. Prochlorococcus and Synechococcus assimilated glucose, leucine and ATP at all stations, but cell‐specific assimilation rates of N and P containing molecules were significantly higher than glucose. Incubations in the dark or with an inhibitor of photosystem II resulted in reduced assimilation rates. Light‐enhanced cell‐specific glucose uptake was generally higher for cyanobacteria (∼50%) than for the low nucleic acid fraction of bacterioplankton (LNA, ∼35%). Our results confirm previous findings, based mainly on cultures and genomic potentials, showing that Prochlorococcus and Synechococcus have a flexible mixotrophic metabolism, but demonstrate that natural populations remain primarily photoautotrophs. Our findings indicate that mixotrophy by marine cyanobacteria is more likely to be an adaptation to low inorganic nutrient availability rather than a facultative pathway for carbon acquisition.
Studies investigating the fate of diazotrophs through the microbial food web are lacking, although N2 fixation can fuel up to 50 % of new production in some oligotrophic oceans. In particular, the ...role played by heterotrophic prokaryotes in this transfer is largely unknown. In the frame of the VAHINE (VAriability of vertical and tropHIc transfer of diazotroph derived N in the south wEst Pacific) experiment, three replicate large-volume (∼ 50 m3) mesocosms were deployed for 23 days in the new Caledonia lagoon and were intentionally fertilized on day 4 with dissolved inorganic phosphorus (DIP) to stimulate N2 fixation. We specifically examined relationships between heterotrophic bacterial production (BP) and N2 fixation or primary production, determined bacterial growth efficiency and established carbon budgets. BP was statistically higher during the second phase of the experiment (P2: days 15–23), when chlorophyll biomass started to increase compared to the first phase (P1: days 5–14). Phosphatase alkaline activity increased drastically during the second phase of the experiment, showing adaptations of microbial populations after utilization of the added DIP. Notably, among autotrophs, Synechococcus abundances increased during P2, possibly related to its capacity to assimilate leucine and to produce alkaline phosphatase. Bacterial growth efficiency based on the carbon budget (27–43 %), was notably higher than generally cited for oligotrophic environments and discussed in links with the presence of abundant species of bacteria expressing proteorhodopsin. The main fates of gross primary production (particulate + dissolved) were respiration (67 %) and export through sedimentation (17 %). BP was highly correlated with particulate primary production and chlorophyll biomass during both phases of the experiment but was slightly correlated, and only during P2 phase, with N2 fixation rates. Heterotrophic bacterial production was strongly stimulated after mineral N enrichment experiments, suggesting N-limitation of heterotrophic bacteria across the experiment. N2 fixation rates corresponded to 17–37 % of the nitrogen demand of heterotrophic bacteria. Our results suggest that most of the diazotroph-derived nitrogen fuelled the heterotrophic bacterial community through indirect processes generating dissolved organic matter and detritus, like mortality, lysis and grazing of both diazotrophs and non-diazotrophs.
In the framework of the VAHINE project, we investigated the spectral characteristics and the variability of dissolved and particulate chromophoric materials throughout a 23-day mesocosm experiment ...conducted in the south-west Pacific at the mouth of the New Caledonian coral lagoon (22°29.073 S–166°26.905 E) from 13 January to 4 February 2013. Samples were collected in a mesocosm fertilized with phosphate at depths of 1, 6 and 12 m and in the surrounding waters. Light absorption coefficients of chromophoric dissolved organic matter (CDOM) ag(λ) and particulate matter ap(λ) were determined using a point-source integrating-cavity absorption meter (PSICAM), while fluorescent DOM (FDOM) components were determined from excitation-emission matrices (EEMs) combined with parallel factor analysis (PARAFAC). The evolutions of ag(λ) and ap(λ) in the mesocosm were similar to those of total chlorophyll a concentration, Synechococcus spp. and picoeukaryote abundances, bacterial production, particulate organic nitrogen and total organic carbon concentrations, with roughly a decrease from the beginning of the experiment to days 9–10, and an increase from days 9–10 to the end of the experiment. In the surrounding waters, the same trend was observed but the increase was much less pronounced, emphasizing the effect of the phosphate fertilization on the mesocosm's plankton community. Correlations suggested that both Synechococcus cyanobacteria and heterotrophic bacteria were strongly involved in the production of CDOM and absorption of particulate matter. The increase in phytoplankton biomass during the second part of the experiment led to a higher contribution of particulate material in the absorption budget at 442 nm. The three FDOM components identified (tryptophan-, tyrosine- and ultraviolet C (UVC) humic-like fluorophores) did not follow the evolution of CDOM and particulate matter, suggesting they were driven by different production/degradation processes. Finally, the results of this work support the idea there is indirect coupling between the dynamics of N2 fixation and that of chromophoric material via the stimulation of Synechococcus bloom.
The deep chlorophyll maximum (DCM) is a ubiquitous feature of phytoplankton vertical distribution in stratified waters that is relevant to our understanding of the mechanisms that underpin the ...variability in photoautotroph ecophysiology across environmental gradients and has implications for remote sensing of aquatic productivity. During the PEACETIME (Process studies at the air-sea interface after dust deposition in the Mediterranean Sea) cruise, carried out from 10 May to 11 June 2017, we obtained 23 concurrent vertical profiles of phytoplankton chlorophyll a, carbon biomass and primary production, as well as heterotrophic prokaryotic production, in the western and central Mediterranean basins. Our main aims were to quantify the relative role of
photoacclimation and enhanced growth as underlying mechanisms of the DCM and to assess the trophic coupling between phytoplankton and heterotrophic prokaryotic production. We found that the DCM coincided with a maximum in both the biomass and primary production but not in the growth rate of phytoplankton, which averaged 0.3 d−1 and was relatively constant across the euphotic layer. Photoacclimation explained most of the increased chlorophyll a at the DCM, as the ratio of carbon to chlorophyll a (C:Chl a) decreased from ca. 90–100 (g:g) at the surface to 20–30 at the base of the euphotic layer, while phytoplankton carbon biomass increased from ca. 6 mg C m−3 at the surface to 10–15 mg C m−3 at the DCM. As a result of photoacclimation, there was an uncoupling between chlorophyll a-specific and carbon-specific productivity across the euphotic layer. The ratio of fucoxanthin to total chlorophyll a increased markedly with depth, suggesting an increased contribution of diatoms at the DCM. The increased biomass and carbon fixation at the base of the euphotic zone was associated with enhanced rates of heterotrophic prokaryotic activity, which also showed a surface peak linked with warmer temperatures. Considering the phytoplankton biomass and turnover rates measured at the DCM, nutrient diffusive fluxes across the nutricline were able to supply only a minor fraction of the
photoautotroph nitrogen and phosphorus requirements. Thus the deep maxima in biomass and primary production were not fuelled by new nutrients but likely resulted from cell sinking from the upper layers in combination with the high photosynthetic efficiency of a diatom-rich, low-light acclimated community largely sustained by regenerated nutrients. Further studies with increased temporal and spatial resolution will be required to ascertain if the peaks of deep primary production associated with the DCM persist across the western and central Mediterranean Sea throughout the stratification season.
Hydrolysis of dissolved organic phosphorus by marine planktonic microorganisms is a key process in the P cycle, particularly in P-depleted, oligotrophic environments. The present study assessed ...spatiotemporal variations in phosphomonoesterase (PME) and phosphodiesterase (PDE) activities using concentration kinetics in the eastern Mediterranean Sea in two contrasting situations: the end of winter (including a small bloom period) and autumn. The distribution and regulation of the maximum hydrolysis rate (Vm) and half-saturation constant (Km) of both ectoenzymes were assessed in relation to the vertical structure of the epipelagic layers. PME reached its maximum activities (Vm) after the addition of 1 µM MUF-P (4-methylumbelliferyl phosphate), whereas, for PDE, it was necessary to add up to 50 µM bis(4-methylumbelliferyl)phosphate (bis-MUF-P) to reach saturation state. On average, the Km of PDE was 33 ± 25 times higher than that of PME. The Vm of PME and Vm of PDE were linearly correlated. Conversely to the Km values, Vm values were on the same order of magnitude for both ectoenzymes, with their ratio (Vm PME : Vm PDE) ranging between 0.2 and 6.3. Dissolved organic phosphorus (DOP) and the phosphomonoesterase hydrolysable fraction of DOP explained most of the lack of variability in Vm PME and Vm PDE. On the contrary, Vm of both phosphohydrolase enzymes was inversely correlated to the concentration of dissolved inorganic phosphorus. The particular characteristics of concentration kinetics obtained for PDE (saturation at 50 µM, high Km, high turnover times) are discussed with respect to the possible unequal distribution of PDE and PME among the size continuum of organic material and accessibility of phosphodiesters.
Oligotrophic regions play a central role in global biogeochemical cycles, with microbial communities in these areas representing an important term in global carbon budgets. While the general ...structure of microbial communities has been well documented in the global ocean, some remote regions such as the western tropical South Pacific (WTSP) remain fundamentally unexplored. Moreover, the biotic and abiotic factors constraining microbial abundances and distribution remain not well resolved. In this study, we quantified the spatial (vertical and horizontal) distribution of major microbial plankton groups along a transect through the WTSP during the austral summer of 2015, capturing important autotrophic and heterotrophic assemblages including cytometrically determined abundances of non-pigmented protists (also called flagellates). Using environmental parameters (e.g., nutrients and light availability) as well as statistical analyses, we estimated the role of bottom–up and top–down controls in constraining the structure of the WTSP microbial communities in biogeochemically distinct regions. At the most general level, we found a “typical tropical structure”, characterized by a shallow mixed layer, a clear deep chlorophyll maximum at all sampling sites, and a deep nitracline. Prochlorococcus was especially abundant along the transect, accounting for 68 ± 10.6 % of depth-integrated phytoplankton biomass. Despite their relatively low abundances, picophytoeukaryotes (PPE) accounted for up to 26 ± 11.6 % of depth-integrated phytoplankton biomass, while Synechococcus accounted for only 6 ± 6.9 %. Our results show that the microbial community structure of the WTSP is typical of highly stratified regions, and underline the significant contribution to total biomass by PPE populations. Strong relationships between N2 fixation rates and plankton abundances demonstrate the central role of N2 fixation in regulating ecosystem processes in the WTSP, while comparative analyses of abundance data suggest microbial community structure to be increasingly regulated by bottom–up processes under nutrient limitation, possibly in response to shifts in abundances of high nucleic acid bacteria (HNA).
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