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Sophie Bonnet - One of the best experts on this subject based on the ideXlab platform.
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Bleaching forces coral’s heterotrophy on Diazotrophs and Synechococcus
The ISME Journal, 2019Co-Authors: Valentine Meunier, Sophie Bonnet, Olivier Grosso, Mar Benavides, Anne Lorrain, Mathieu Pernice, Christophe Lambert, Fanny HoulbrèqueAbstract:Coral reefs are threatened by global warming, which disrupts the symbiosis between corals and their photosynthetic symbionts (Symbiodiniaceae), leading to mass coral bleaching. Planktonic Diazotrophs or dinitrogen (N2)-fixing prokaryotes are abundant in coral lagoon waters and could be an alternative nutrient source for corals. Here we incubated untreated and bleached coral colonies of Stylophora pistillata with a 15N2-pre-labelled natural plankton assemblage containing Diazotrophs. 15N2 assimilation rates in Symbiodiniaceae cells and tissues of bleached corals were 5- and 30-fold higher, respectively, than those measured in untreated corals, demonstrating that corals incorporate more nitrogen derived from planktonic Diazotrophs under bleaching conditions. Bleached corals also preferentially fed on Synechococcus, nitrogen-rich picophytoplanktonic cells, instead of Prochlorococcus and picoeukaryotes, which have a lower cellular nitrogen content. By providing an alternative source of bioavailable nitrogen, both the incorporation of nitrogen derived from planktonic Diazotrophs and the ingestion of Synechococcus may have profound consequences for coral bleaching recovery, especially for the many coral reef ecosystems characterized by high abundance and activity of planktonic Diazotrophs.
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biogeochemical fluxes and fate of Diazotroph derived nitrogen in the food web after a phosphate enrichment modeling of the vahine mesocosms experiment
Biogeosciences, 2016Co-Authors: Audrey Gimenez, Sophie Bonnet, Melika Baklouti, Thierry MoutinAbstract:Abstract. The VAHINE mesocosm experiment in the oligotrophic waters of the Noumea lagoon (New Caledonia), where high N2 fixation rates and abundant Diazotroph organisms were observed, aimed to assess the role of the nitrogen input through N2 fixation in carbon production and export and to study the fate of Diazotroph-derived nitrogen (DDN) throughout the planktonic food web. A 1-D vertical biogeochemical mechanistic model was used in addition to the in situ experiment to enrich our understanding of the dynamics of the planktonic ecosystem and the main biogeochemical carbon (C), nitrogen (N) and phosphate (P) fluxes. The mesocosms were intentionally enriched with ∼ 0.8 µmol L−1 of inorganic P to trigger the development of Diazotrophs and amplify biogeochemical fluxes. Two simulations were run, one with and the other without the phosphate enrichment. In the P-enriched simulation, N2 fixation, primary production (PP) and C export increased by 201, 208 and 87 %, respectively, consistent with the trends observed in the mesocosms (+124, +141 and +261 % for N2 fixation, PP and C export, respectively). In total, 5–10 days were necessary to obtain an increase in primary and export productions after the dissolved inorganic phosphate (DIP) enrichment, thereby suggesting that classical methods (short-term microcosms experiments) used to quantify nutrient limitations of primary production may not be relevant. The model enabled us to monitor the fate of fixed N2 by providing the proportion of DDN in each compartment (inorganic and organic) of the model over time. At the end of the simulation (25 days), 43 % of the DDN was found in the non-Diazotroph organisms, 33 % in Diazotrophs, 16 % in the dissolved organic nitrogen pool, 3 % in the particulate detrital organic pool and 5 % in traps, indicating that N2 fixation was of benefit to non-Diazotrophic organisms and contributed to C export.
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biogeochemical and biological impacts of Diazotroph blooms in a low nutrient low chlorophyll ecosystem synthesis from the vahine mesocosm experiment new caledonia
Biogeosciences, 2016Co-Authors: H Berthelot, Sophie Bonnet, Melika Baklouti, Audrey Gimenez, Ilana BermanfrankAbstract:Abstract. 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.
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transfer of Diazotroph derived nitrogen towards non Diazotrophic planktonic communities a comparative study between trichodesmium erythraeum crocosphaera watsonii and cyanothece sp
Biogeosciences, 2016Co-Authors: H Berthelot, Sophie Bonnet, Olivier Grosso, Veronique Cornet, Aude BaraniAbstract:Abstract. Biological dinitrogen (N2) fixation is the major source of new nitrogen (N) for the open ocean, and thus promotes marine productivity, in particular in the vast N-depleted regions of the surface ocean. Yet, the fate of the Diazotroph-derived N (DDN) in marine ecosystems is poorly understood, and its transfer to auto- and heterotrophic surrounding plankton communities is rarely measured due to technical limitations. Moreover, the different Diazotrophs involved in N2 fixation (Trichodesmium spp. vs. UCYN) exhibit distinct patterns of N2 fixation and inhabit different ecological niches, thus having potentially different fates in the marine food webs that remain to be explored. Here we used 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 artificially induced Diazotroph blooms in New Caledonia (southwestern Pacific). The fate of the DDN was compared according to the three Diazotrophs: the filamentous and colony-forming Trichodesmium erythraeum (IMS101), and the unicellular strains Crocosphaera watsonii WH8501 and Cyanothece ATCC51142. After 48 h, 7–17 % of the N2 fixed during the experiment was transferred to the dissolved pool and 6–12 % was transferred to non-Diazotrophic plankton. The transfer was twice as high in the T. erythraeum bloom than in the C. watsonii and Cyanothece blooms, which shows that filamentous Diazotrophs blooms are more efficient at promoting non-Diazotrophic production in N-depleted areas. The amount of DDN released in the dissolved pool did not appear to be a good indicator of the DDN transfer efficiency towards the non-Diazotrophic plankton. In contrast, the 15N-enrichment of the extracellular ammonium (NH4+) pool was a good indicator of the DDN transfer efficiency: it was significantly higher in the T. erythraeum than in unicellular Diazotroph blooms, leading to a DDN transfer twice as efficient. This suggests that NH4+ was the main pathway of the DDN transfer from Diazotrophs to non-Diazotrophs. The three simulated Diazotroph blooms led to significant increases in non-Diazotrophic plankton biomass. This increase in biomass was first associated with heterotrophic bacteria followed by phytoplankton, indicating that heterotrophs took the most advantage of the DDN in this oligotrophic ecosystem.
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Diazotrophs: a non-negligible source of nitrogen for the tropical coral Stylophora pistillata.
The Journal of experimental biology, 2016Co-Authors: Mar Benavides, Olivier Grosso, Fanny Houlbrèque, Mercedes Camps, Anne Lorrain, Sophie BonnetAbstract:Corals are mixotrophs: they are able to fix inorganic carbon through the activity of their symbiotic dinoflagellates and to gain nitrogen from predation on plankton and uptake of dissolved organic and inorganic nutrients. They also live in close association with diverse Diazotrophic communities, inhabiting their skeleton, tissue and mucus layer, which are able to fix dinitrogen (N2). The quantity of fixed N2 transferred to the corals and its distribution within coral compartments as well as the quantity of nitrogen assimilated through the ingestion of planktonic Diazotrophs are still unknown. Here, we quantified nitrogen assimilation via (i) N2 fixation by symbiont Diazotrophs, (ii) ingestion of cultured unicellular Diazotrophs and (iii) ingestion of natural planktonic Diazotrophs. We estimate that the ingestion of Diazotrophs provides 0.76±0.15 µg N cm(-2) h(-1), suggesting that Diazotrophs represent a non-negligible source of nitrogen for scleractinian corals.
Jonathan P. Zehr - One of the best experts on this subject based on the ideXlab platform.
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Distribution and activity of Diazotrophs in the Eastern
2020Co-Authors: Equatorial Atlantic, Rachel A Foster, Ajit Subramaniam, Jonathan P. ZehrAbstract:Summary The gene abundance and gene expression of six Diazotroph populations from the Eastern Equatorial Atlantic in June 2007 were examined using nifH gene quantitative polymerase chain reaction (q PCR) methods. Of all the Diazotrophs, Trichodesmium spp. was the most abundant with the highest number of gene copies in the Gulf of Guinea. Trichodesmium also had the highest nitrogenase gene transcript abundance overall with the maximum in samples collected at the equator and in waters influenced by the Congo River plume (> 10 5 cDNA nifH copies l -1 ). Both cyanobacterial unicellular groups (A and B) were detected, where group A was the second most abundant in surface samples, in particular at the stations along the equator. Transcript abundance for group A, however, was at the detection limit and suggests that it was not actively fixing N2. Trichodesmium and group B nifH gene abundances co-varied (P 10 4 nifH copies l -1 ) were found north-west of the Congo River plume. In contrast, the Calothrix symbionts (het-3) of Chaetoceros had low abundances at the surface, but were present at 3.7 ¥ 10 4 nifH copies l -1 at 40 m depth in the equatorial upwelling. This is the first report of the Calothrix symbiont in the Atlantic Ocean. This is also the first report of nifH gene copy and transcript abundance in an Equatorial upwelling zone. Although the number of gene copies for Richelia associated with Rhizosolenia were the lowest, the transcript abundance were high (9.4 ¥ 10 1 -1.8 ¥ 10 4 cDNA nifH copies l -1 ) and similar to that of Trichodesmium. The distribution of the Diazotroph groups, especially the three strains of symbiotic cyanobacteria, was different, and appeared largely controlled by riverine inputs and upwelling.
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periodic and coordinated gene expression between a Diazotroph and its diatom host
The ISME Journal, 2019Co-Authors: Matthew J Harke, Jonathan P. Zehr, Sonya T. Dyhrman, Sheean T. Haley, Kyle R Frischkorn, Frank O AylwardAbstract:In the surface ocean, light fuels photosynthetic carbon fixation of phytoplankton, playing a critical role in ecosystem processes including carbon export to the deep sea. In oligotrophic oceans, diatom–Diazotroph associations (DDAs) play a keystone role in ecosystem function because Diazotrophs can provide otherwise scarce biologically available nitrogen to the diatom host, fueling growth and subsequent carbon sequestration. Despite their importance, relatively little is known about the nature of these associations in situ. Here we used metatranscriptomic sequencing of surface samples from the North Pacific Subtropical Gyre (NPSG) to reconstruct patterns of gene expression for the Diazotrophic symbiont Richelia and we examined how these patterns were integrated with those of the diatom host over day–night transitions. Richelia exhibited significant diel signals for genes related to photosynthesis, N2 fixation, and resource acquisition, among other processes. N2 fixation genes were significantly co-expressed with host nitrogen uptake and metabolism, as well as potential genes involved in carbon transport, which may underpin the exchange of nitrogen and carbon within this association. Patterns of expression suggested cell division was integrated between the host and symbiont across the diel cycle. Collectively these data suggest that symbiont–host physiological ecology is strongly interconnected in the NPSG.
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in situ Diazotroph population dynamics under different resource ratios in the north pacific subtropical gyre
Frontiers in Microbiology, 2018Co-Authors: Kendra A Turkkubo, M. E. Hogan, Paige E Connell, David A Caron, Hanna Farnelid, Jonathan P. ZehrAbstract:Author(s): Turk-Kubo, Kendra A; Connell, Paige; Caron, David; Hogan, Mary E; Farnelid, Hanna M; Zehr, Jonathan P | Abstract: Major advances in understanding the diversity, distribution, and activity of marine N2-fixing microorganisms (Diazotrophs) have been made in the past decades, however, large gaps in knowledge remain about the environmental controls on growth and mortality rates. In order to measure Diazotroph net growth rates and microzooplankton grazing rates on Diazotrophs, nutrient perturbation experiments and dilution grazing experiments were conducted using free-floating in situ incubation arrays in the vicinity of Station ALOHA in March 2016. Net growth rates for targeted Diazotroph taxa as well as Prochlorococcus, Synechococcus and photosynthetic picoeukaryotes were determined under high (H) and low (L) nitrate:phosphate (NP) ratio conditions at four depths in the photic zone (25, 45, 75, and 100 m) using quantitative PCR and flow cytometry. Changes in the prokaryote community composition in response to HNP and LNP treatments were characterized using 16S rRNA variable region tag sequencing. Microzooplankton grazing rates on Diazotrophs were measured using a modified dilution technique at two depths in the photic zone (15 and 125 m). Net growth rates for most of the targeted Diazotrophs after 48 h were not stimulated as expected by LNP conditions, rather enhanced growth rates were often measured in HNP treatments. Interestingly, net growth rates of the uncultivated prymnesiophyte symbiont UCYN-A1 were stimulated in HNP treatments at 75 and 100 m, suggesting that N used for growth was acquired through continuing to fix N2 in the presence of nitrate. Net growth rates for UCYN-A1, UCYN-C, Crocosphaera sp. (UCYN-B) and the diatom symbiont Richelia (associated with Rhizosolenia) were uniformly high at 45 m (up to 1.6 ± 0.5 d-1), implying that all were growing optimally at the onset of the experiment at that depth. Differences in microzooplankton grazing rates on UCYN-A1 and UCYN-C in 15 m waters indicate that the grazer assemblage preyed preferentially on UCYN-A1. Deeper in the water column (125 m), both Diazotrophs were grazed at substantial rates, suggesting grazing pressure may increase with depth in the photic zone. Constraining in situ Diazotroph growth and mortality rates are important steps for improving parameterization for Diazotrophs in global ecosystem models.
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Diazotroph community succession during the vahine mesocosm experiment new caledonia lagoon
Biogeosciences, 2015Co-Authors: Kendra A Turkkubo, Sophie Bonnet, I. E. Frank, M. E. Hogan, A. Desnues, Jonathan P. ZehrAbstract:The VAHINE mesocosm experiment, conducted in the low-nutrient low-chlorophyll waters of the Noumea lagoon (coastal New Caledonia) was designed to trace the incorporation of nitrogen (N) fixed by Diazotrophs into the food web, using large volume (50 m 3 / mesocosms. This ex- periment provided a unique opportunity to study the succes- sion of different N2-fixing microorganisms (Diazotrophs) and calculate in situ net growth and mortality rates in response to fertilization with dissolved inorganic phosphate (DIP) over a 23-day period, using quantitative polymerase chain reac- tion (qPCR) assays targeting widely distributed marine di- azotroph lineages. Inside the mesocosms, the most abun- dant Diazotroph was the heterocyst-forming Richelia asso- ciated with Rhizosolenia (Het-1) in the first half of the ex- periment, while unicellular cyanobacterial Group C (UCYN- C) became abundant during the second half of the exper- iment. Decreasing DIP concentrations following the fertil- ization event and increasing temperatures were significantly correlated with increasing abundances of UCYN-C. Maxi- mum net growth rates for UCYN-C were calculated to range between 1.23 0.07 and 2.16 0.07 d 1 in the mesocosms, which are among the highest growth rates reported for dia- zotrophs. Outside the mesocosms in the New Caledonia la- goon, UCYN-C abundances remained low, despite increas- ing temperatures, suggesting that the microbial community response to the DIP fertilization created conditions favorable for UCYN-C growth inside the mesocosms. Diazotroph com- munity composition analysis using PCR targeting a compo- nent of the nitrogenase gene (nifH) verified that Diazotrophs targeted in qPCR assays were collectively among the ma- jor lineages in the lagoon and mesocosm samples, with the exception of Crocosphaera-like phylotypes, where sequence types not typically seen in the oligotrophic ocean grew in the mesocosms. Maximum net growth and mortality rates for nine Diazotroph phylotypes throughout the 23-day exper- iment were variable between mesocosms, and repeated fluc- tuations between periods of net growth and mortality were commonly observed. The field population of Diazotrophs in the New Caledonian lagoon waters appeared to be domi- nated by Het-1 over the course of the study period. How- ever, results from both qPCR and PCR analysis indicated a diverse field population of Diazotrophs was present in the la- goon at the time of sampling. Two ecotypes of the Braaru- dosphaera bigelowii symbiont unicellular group A (UCYN- A) were present simultaneously in the lagoon, with the re- cently described B. bigelowii/UCYN-A2 association present at higher abundances than the B. bigelowii/UCYN-A1 asso- ciation.
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Gammaproteobacterial Diazotrophs and nifH gene expression in surface waters of the South Pacific Ocean
The ISME Journal, 2014Co-Authors: Pia H Moisander, Ryan W. Paerl, Tracy Serros, Roxanne A Beinart, Jonathan P. ZehrAbstract:In addition to the cyanobacterial N_2-fixers (Diazotrophs), there is a high nifH gene diversity of non-cyanobacterial groups present in marine environments, yet quantitative information about these groups is scarce. N_2 fixation potential ( nifH gene expression), diversity and distributions of the uncultivated Diazotroph phylotype γ-24774A11, a putative gammaproteobacterium, were investigated in the western South Pacific Ocean. γ-24774A11 gene copies correlated positively with Diazotrophic cyanobacteria, temperature, dissolved organic carbon and ambient O_2 saturation, and negatively with depth, chlorophyll a and nutrients, suggesting that carbon supply, access to light or inhibitory effects of DIN may control γ-24774A11 abundances. Maximum nifH gene-copy abundance was 2 × 10^4 l^−1, two orders of magnitude less than that for Diazotrophic cyanobacteria, while the median γ-24774A11 abundance, 8 × 10^2 l^−1, was greater than that for the UCYN-A cyanobacteria, suggesting a more homogeneous distribution in surface waters. The abundance of nifH transcripts by γ-24774A11 was greater during the night than during the day, and the transcripts generally ranged from 0–7%, but were up to 26% of all nifH transcripts at each station. The ubiquitous presence and low variability of γ-24774A11 abundances across tropical and subtropical oceans, combined with the consistent nifH expression reported in this study, suggest that γ-24774A11 could be one of the most important heterotrophic (or photoheterotrophic) Diazotrophs and may need to be considered in future N budget estimates and models.
Charles R. Lovell - One of the best experts on this subject based on the ideXlab platform.
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responses of salt marsh plant rhizosphere Diazotroph assemblages to drought
Microorganisms, 2018Co-Authors: Debra A. Davis, Sparkle L Malone, Charles R. LovellAbstract:Drought has many consequences in the tidally dominated Spartina sp. salt marshes of the southeastern US; including major dieback events, changes in sediment chemistry and obvious changes in the landscape. These coastal systems tend to be highly productive, yet many salt marshes are also nitrogen limited and depend on plant associated Diazotrophs as their source of ‘new’ nitrogen. A 4-year study was conducted to investigate the structure and composition of the rhizosphere Diazotroph assemblages associated with 5 distinct plant zones in one such salt marsh. A period of greatly restricted tidal inundation and precipitation, as well as two periods of drought (June–July 2004, and May 2007) occurred during the study. DGGE of nifH PCR amplicons from rhizosphere samples, Principal Components Analysis of the resulting banding patterns, and unconstrained ordination analysis of taxonomic data and environmental parameters were conducted. Diazotroph assemblages were organized into 5 distinct groups (R2 = 0.41, p value < 0.001) whose presence varied with the environmental conditions of the marsh. Diazotroph assemblage group detection differed during and after the drought event, indicating that persistent Diazotrophs maintained populations that provided reduced supplies of new nitrogen for vegetation during the periods of drought.
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Specificity of Salt Marsh Diazotrophs for Vegetation Zones and Plant Hosts: Results from a North American marsh.
Frontiers in Microbiology, 2012Co-Authors: Charles R. Lovell, Debra A. DavisAbstract:Salt marshes located on the east coast of temperate North America are highly productive, typically nitrogen-limited, and support diverse assemblages of nitrogen fixing (Diazotrophic) bacteria. The distributions of these Diazotrophs are strongly influenced by plant host and abiotic environmental parameters. Crab Haul Creek Basin, North Inlet, SC, USA is a tidally dominated marsh that displays discrete plant zones distributed along an elevation gradient from the tidal creek bank to the terrestrial forest. These zones are defined by gradients of abiotic environmental variables, particularly salinity and sulfide. DGGE fingerprinting and phylogenetic analyses of recovered sequences demonstrated that the distributions of some Diazotrophs indicate plant host specificity and that Diazotroph assemblages across the marsh gradient are heavily influenced by edaphic conditions. Broadly distributed Diazotrophs capable of maintaining populations in all environmental conditions across the gradient are also present in these assemblages. Parsimony test results confirm that Diazotroph assemblages in different plant zones are significantly (p
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Responses of salt marsh plant rhizosphere Diazotroph assemblages to changes in marsh elevation, edaphic conditions and plant host species.
Microbial Ecology, 2010Co-Authors: Debra A. Davis, Christopher E Bagwell, Megan D. Gamble, Peter W. Bergholz, Charles R. LovellAbstract:An important source of new nitrogen in salt marsh ecosystems is microbial Diazotrophy (nitrogen fixation). The Diazotroph assemblages associated with the rhizospheres (sediment directly affected by the roots) of salt marsh plants are highly diverse, somewhat stable, and consist mainly of novel organisms. In Crab Haul Creek Basin, North Inlet, SC, the distribution of plant types into discrete zones is dictated by relatively minor differences in marsh elevation and it was hypothesized that the biotic and abiotic properties of the plant zones would also dictate the composition of the rhizosphere Diazotroph assemblages. Over a period of 1 year, rhizosphere sediments were collected from monotypic stands of the black needlerush, Juncus roemerianus, the common pickleweed, Salicornia virginica, the short and tall growth forms of the smooth cordgrass Spartina alterniflora, and a mixed zone of co-occurring S. virginica and short form, S. alterniflora. DNA was extracted, purified and nifH sequences PCR amplified for denaturing gradient gel electrophoresis (DGGE) analysis to determine the composition of the Diazotroph assemblages. The Diazotroph assemblages were strongly influenced by season, abiotic environmental parameters and plant host. Sediment chemistry and nitrogen fixation activity were also significantly influenced by seasonal changes. DGGE bands that significantly affected seasonal and zone specific clustering were identified and most of these sequences were from novel Diazotrophs, unaffiliated with any previously described organisms. At least one third of the recovered nifH sequences were from a diverse assemblage of Chlorobia, and γ-, α-, β- and δ-Proteobacteria. Diazotrophs that occurred throughout the growing season and among all zones (frequently detected) were also mostly novel. These significant sequences indicated that Diazotrophs driving the structure of the assemblages were diverse, versatile, and some were ubiquitous while others were seasonally responsive. Several ubiquitous sequences were closely related to sequences of actively N2 fixing Diazotrophs previously recovered from this system. These sequences from ubiquitous and versatile organisms likely indicate the Diazotrophs in these rhizosphere assemblages that significantly contribute to ecosystem function.
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seasonal variability of Diazotroph assemblages associated with the rhizosphere of the salt marsh cordgrass spartina alterniflora
Microbial Ecology, 2010Co-Authors: Megan D. Gamble, Christopher E Bagwell, Peter W. Bergholz, Jeannine R Larocque, Charles R. LovellAbstract:Nitrogen fixation is the primary N source in the highly productive but N-limited North Inlet, SC, USA salt marsh system. The diverse assemblages of nitrogen-fixing (Diazotrophic) bacteria associated with the rhizospheres of the short and tall growth forms of Spartina alterniflora were analyzed at two sites, Crab Haul Creek and Goat Island, which are in different tidal creek drainage systems in this marsh. The sites differed in proximity to the main channel for tidal intrusion and in several edaphic parameters. We hypothesized that either the differing abiotic environmental regimes of the two sites or the variation due to seasonal effects result in differences in the Diazotroph assemblage. Rhizosphere samples were collected seasonally during 1999 and 2000. DNA was purified and nifH amplified for denaturing gradient gel electrophoresis (DGGE) analysis of Diazotroph assemblage composition. Principal components analysis was used to analyze the binary DGGE band position data. Season strongly influenced assemblage composition and biplots were used to identify bands that significantly affected the seasonal and site-specific clustering. The types of organisms that were most responsive to seasonal or site variability were identified on the basis of DGGE band sequences. Seasonally responsive members of the anaerobic Diazotrophs were detected during the winter and postsenescence conditions and may have been responsible for elevated pore water sulfide concentrations. Sequences from a diverse assemblage of Gammaproteobacteria were predominant during growth periods of S. alterniflora. Abiotic environmental parameters strongly influenced both the S. alterniflora and the Diazotrophic bacterial assemblages associated with this keystone salt marsh plant species.
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Persistence of selected Spartina alterniflora rhizoplane Diazotrophs exposed to natural and manipulated environmental variability.
Applied and Environmental Microbiology, 2000Co-Authors: Christopher E Bagwell, Charles R. LovellAbstract:Rhizoplane-rhizosphere nitrogen-fixing microorganisms (Diazotrophs) are thought to provide a major source of biologically available nitrogen in salt marshes dominated by Spartina alterniflora. Compositional and functional stability has been demonstrated for this important functional group; however, the quantitative responses of specific Diazotroph populations to environmental variability have not been assessed. Changes in the relative abundances of selected rhizoplane Diazotrophs in response to long-term fertilization were monitored quantitatively by reverse sample genome probing. Fertilization stimulated Spartina, with plant height nearly tripling after 1 year. Fertilization also resulted in significant changes in interstitial porewater parameters. Diazotrophic activity (acetylene reduction assay) was sensitive to the fertilization treatments and was inhibited in some plots on several sampling dates. However, inhibition was never consistent across all of the replicates within a treatment and activity always recovered. The rhizoplane Diazotrophs were quite responsive to environmental variability and to experimental treatments, but none were displaced by either environmental variability or experimental treatments. All strains were detected consistently throughout this study, and extensive spatial heterogeneity in the distribution patterns of these organisms was observed. The physiological traits that differentiate the Diazotroph populations presumably support competitiveness and niche specialization, resulting in the observed resilience of the Diazotroph populations in the rhizosphere.
Sonya T. Dyhrman - One of the best experts on this subject based on the ideXlab platform.
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periodic and coordinated gene expression between a Diazotroph and its diatom host
The ISME Journal, 2019Co-Authors: Matthew J Harke, Jonathan P. Zehr, Sonya T. Dyhrman, Sheean T. Haley, Kyle R Frischkorn, Frank O AylwardAbstract:In the surface ocean, light fuels photosynthetic carbon fixation of phytoplankton, playing a critical role in ecosystem processes including carbon export to the deep sea. In oligotrophic oceans, diatom–Diazotroph associations (DDAs) play a keystone role in ecosystem function because Diazotrophs can provide otherwise scarce biologically available nitrogen to the diatom host, fueling growth and subsequent carbon sequestration. Despite their importance, relatively little is known about the nature of these associations in situ. Here we used metatranscriptomic sequencing of surface samples from the North Pacific Subtropical Gyre (NPSG) to reconstruct patterns of gene expression for the Diazotrophic symbiont Richelia and we examined how these patterns were integrated with those of the diatom host over day–night transitions. Richelia exhibited significant diel signals for genes related to photosynthesis, N2 fixation, and resource acquisition, among other processes. N2 fixation genes were significantly co-expressed with host nitrogen uptake and metabolism, as well as potential genes involved in carbon transport, which may underpin the exchange of nitrogen and carbon within this association. Patterns of expression suggested cell division was integrated between the host and symbiont across the diel cycle. Collectively these data suggest that symbiont–host physiological ecology is strongly interconnected in the NPSG.
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Phosphorus scavenging in the unicellular marine Diazotroph Crocosphaera watsonii.
Applied and Environmental Microbiology, 2006Co-Authors: Sonya T. Dyhrman, Sheean T. HaleyAbstract:Phytoplankton, including cyanobacteria from the genera Prochlorococcus, Synechococcus, Crocosphaera, and Trichodesmium, significantly contribute to overall marine primary production and thereby play a key role in the global cycling of carbon (C). Within the cyanobacteria, Diazotrophs, such as Trichodesmium, are particularly important because of their ability to fix atmospheric nitrogen (N). Although Trichodesmium is perhaps the best-known and best-studied marine Diazotroph, recent research (18, 31) has highlighted the biogeochemical importance of small, unicellular Diazotrophs (3 to 10 μm), such as Crocosphaera watsonii, which can introduce a substantial fraction of new nitrogen to the euphotic zone in tropical systems where it occurs (3, 5, 9, 18, 31). Much of our knowledge regarding unicellular Diazotrophs, such as C. watsonii, has been driven by recent molecular work to assess the expression of nifH, a dinitrogenase reductase-encoding gene responsible for N2 fixation. This work has led to the identification of two open-ocean nifH sequence types, group A and group B. These sequence groups phylogenetically cluster with unicellular cyanobacteria (9, 10, 31). Group A nifH DNA phylotypes are most closely related to the genus Cyanothece, while group B nifH phylotypes are most similar to Crocosphaera watsonii WH8501 (5, 31). Quantitative PCR to detect nifH has found these phylotypes to be abundant and, at times, more abundant than Trichodesmium spp. in oligotrophic waters (5). While Trichodesmium is typically most abundant in the upper euphotic zone (4), the unicellular Diazotrophs which make up groups A and B have been reported to be more uniformly distributed through the euphotic zone (17, 18). They also differ from Trichodesmium in that they fix nitrogen maximally at night, rather than during the day (31). Ultimately, the diversity, abundance, and widespread distribution of unicellular Diazotrophs culminate in high rates of N2 fixation. The factors that control the growth and N2 fixation rates of marine Diazotrophs have been intensively studied. One of these factors is the bioavailability of phosphorus. Two major ocean biomes, the North Pacific Subtropical Gyre and the Sargasso Sea, have very low inorganic phosphate concentrations (
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phosphorus scavenging in the unicellular marine Diazotroph crocosphaera watsonii
Applied and Environmental Microbiology, 2006Co-Authors: Sonya T. Dyhrman, Sheean T. HaleyAbstract:Phytoplankton, including cyanobacteria from the genera Prochlorococcus, Synechococcus, Crocosphaera, and Trichodesmium, significantly contribute to overall marine primary production and thereby play a key role in the global cycling of carbon (C). Within the cyanobacteria, Diazotrophs, such as Trichodesmium, are particularly important because of their ability to fix atmospheric nitrogen (N). Although Trichodesmium is perhaps the best-known and best-studied marine Diazotroph, recent research (18, 31) has highlighted the biogeochemical importance of small, unicellular Diazotrophs (3 to 10 μm), such as Crocosphaera watsonii, which can introduce a substantial fraction of new nitrogen to the euphotic zone in tropical systems where it occurs (3, 5, 9, 18, 31). Much of our knowledge regarding unicellular Diazotrophs, such as C. watsonii, has been driven by recent molecular work to assess the expression of nifH, a dinitrogenase reductase-encoding gene responsible for N2 fixation. This work has led to the identification of two open-ocean nifH sequence types, group A and group B. These sequence groups phylogenetically cluster with unicellular cyanobacteria (9, 10, 31). Group A nifH DNA phylotypes are most closely related to the genus Cyanothece, while group B nifH phylotypes are most similar to Crocosphaera watsonii WH8501 (5, 31). Quantitative PCR to detect nifH has found these phylotypes to be abundant and, at times, more abundant than Trichodesmium spp. in oligotrophic waters (5). While Trichodesmium is typically most abundant in the upper euphotic zone (4), the unicellular Diazotrophs which make up groups A and B have been reported to be more uniformly distributed through the euphotic zone (17, 18). They also differ from Trichodesmium in that they fix nitrogen maximally at night, rather than during the day (31). Ultimately, the diversity, abundance, and widespread distribution of unicellular Diazotrophs culminate in high rates of N2 fixation. The factors that control the growth and N2 fixation rates of marine Diazotrophs have been intensively studied. One of these factors is the bioavailability of phosphorus. Two major ocean biomes, the North Pacific Subtropical Gyre and the Sargasso Sea, have very low inorganic phosphate concentrations (<1 nM in some cases), high levels of dissolved inorganic N:P, and elevated total dissolved N:P (30). Under these conditions the availability of trace concentrations of dissolved inorganic phosphate (DIP) and the bioavailability of the larger but poorly characterized and chemically heterogeneous pool of dissolved organic phosphorus (DOP) could dramatically influence Diazotroph production and N2 fixation. Several recent studies have identified P bioavailability as a possible controlling factor for the physiology of the Diazotroph Trichodesmium (7, 23); however, P physiology has not yet been examined with cultures or field populations of the unicellular Diazotrophs, such as Crocosphaera. Marine cyanobacteria have evolved a number of different strategies for survival in low-DIP marine systems, such as the North Pacific Subtropical Gyre and the Sargasso Sea. Two common strategies for survival in low-phosphate environments include the induction of high-affinity phosphate scavenging systems and the up-regulation of enzymes to hydrolyze DOP into phosphate. Perhaps the best characterized of these strategies is high-affinity phosphate transport. For example, the gene cluster pstSCAB has been identified in Synechococcus sp. strain WH8102 (26) and Prochlorococcus spp. (19). These genes are up-regulated by P deficiency in Synechocystis sp. strain PCC6803 (27). Also, the presence of the PstS protein can be detected in field populations under low-P conditions (24). Notably absent in the marine cyanobacterial genomes examined to date are any low-affinity phosphate permeases (e.g., pitA) (19, 26). Two of the dominant bond classes of oceanic high-molecular-weight DOP are phosphomonoesters and phosphonates (13). The hydrolysis of phosphomonoesters is mediated by enzymes such as alkaline phosphatase (phoA), the activity of which is commonly up-regulated by P deficiency in cyanobacteria (22). The transport of phosphonates is mediated by phnCDE. This gene cluster is present in all the available Synechococcus and Prochlorococcus genomes (19) and in all the Trichodesmium species examined to date (6). Hydrolysis of phosphonates can be mediated by multiple enzyme systems of different substrate specificities (14). Phosphonate hydrolysis in marine cyanobacteria has not been comprehensively examined, but evidence from Synechococcus sp. strain WH8102 (21, 26) growth studies and Trichodesmium erythraeum gene expression analysis (6) suggests that some marine cyanobacteria may be able to metabolize exogenous phosphonate compounds. Despite these general advances in our understanding of P metabolism in marine cyanobacteria, little is known about how unicellular Diazotrophs, such as C. watsonii, scavenge phosphorus. Here we used a combination of genomic observations and physiological studies to examine P-scavenging strategies of different strains of C. watsonii.
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seasonal resource conditions favor a summertime increase in north pacific diatom Diazotroph associations
The ISME Journal, 2018Co-Authors: Christopher L Follett, Keisuke Inomura, David M Karl, Stephanie Dutkiewicz, Michael J FollowsAbstract:In the North Pacific Subtropical Gyre (NPSG), an annual pulse of sinking organic carbon is observed at 4000 m between July and August, driven by large diatoms found in association with nitrogen fixing, heterocystous, cyanobacteria: Diatom–Diazotroph Associations (DDAs). Here we ask what drives the bloom of DDAs and present a simplified trait-based model of subtropical phototroph populations driven by observed, monthly averaged, environmental characteristics. The ratio of resource supply rates favors nitrogen fixation year round. The relative fitness of DDA traits is most competitive in early summer when the mixed layer is shallow, solar irradiance is high, and phosphorus and iron are relatively abundant. Later in the season, as light intensity drops and phosphorus is depleted, the traits of small unicellular Diazotrophs become more competitive. The competitive transition happens in August, at the time when the DDA export event occurs. This seasonal dynamic is maintained when embedded in a more complex, global-scale, ecological model, and provides predictions for the extent of the North Pacific DDA bloom. The model provides a parsimonious and testable hypothesis for the stimulation of DDA blooms.
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understanding predicted shifts in Diazotroph biogeography using resource competition theory
Biogeosciences, 2014Co-Authors: Stephanie Dutkiewicz, Ben A Ward, Jeffery R Scott, Michael J FollowsAbstract:We examine the sensitivity of the biogeography of nitrogen fixers to a warming climate and increased aeo- lian iron deposition in the context of a global earth system model. We employ concepts from the resource-ratio theory to provide a simplifying and transparent interpretation of the results. First we demonstrate that a set of clearly defined, eas- ily diagnosed provinces are consistent with the theory. Us- ing this framework we show that the regions most vulnera- ble to province shifts and changes in Diazotroph biogeogra- phy are the equatorial and South Pacific, and central Atlantic. Warmer and dustier climates favor Diazotrophs due to an in- crease in the ratio of supply rate of iron to fixed nitrogen. We suggest that the emergent provinces could be a standard diagnostic for global change models, allowing for rapid and transparent interpretation and comparison of model predic- tions and the underlying mechanisms. The analysis suggests that monitoring of real world province boundaries, indicated by transitions in surface nutrient concentrations, would pro- vide a clear and easily interpreted indicator of ongoing global change.
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iron conservation by reduction of metalloenzyme inventories in the marine Diazotroph crocosphaera watsonii
Proceedings of the National Academy of Sciences of the United States of America, 2011Co-Authors: Mak A Saito, Stephanie Dutkiewicz, Michael J Follows, Erin M Bertrand, Vladimir V Bulygin, Dawn M Moran, Fanny M Monteiro, Frederica W Valois, John B WaterburyAbstract:The marine nitrogen fixing microorganisms (Diazotrophs) are a major source of nitrogen to open ocean ecosystems and are predicted to be limited by iron in most marine environments. Here we use global and targeted proteomic analyses on a key unicellular marine Diazotroph Crocosphaera watsonii to reveal large scale diel changes in its proteome, including substantial variations in concentrations of iron metalloproteins involved in nitrogen fixation and photosynthesis, as well as nocturnal flavodoxin production. The daily synthesis and degradation of enzymes in coordination with their utilization results in a lowered cellular metalloenzyme inventory that requires ∼40% less iron than if these enzymes were maintained throughout the diel cycle. This strategy is energetically expensive, but appears to serve as an important adaptation for confronting the iron scarcity of the open oceans. A global numerical model of ocean circulation, biogeochemistry and ecosystems suggests that Crocosphaera’s ability to reduce its iron-metalloenzyme inventory provides two advantages: It allows Crocosphaera to inhabit regions lower in iron and allows the same iron supply to support higher Crocosphaera biomass and nitrogen fixation than if they did not have this reduced iron requirement.
