Trichodesmium

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Sonya T. Dyhrman - One of the best experts on this subject based on the ideXlab platform.

  • <i>Trichodesmium</i> physiological ecology and phosphate reduction in the western Tropical South Pacific
    2018
    Co-Authors: Kyle R. Frischkorn, Andreas Krupke, Mónica Rouco, Andrés E. Salazar Estrada, Benjamin A. S. Van Mooy, Sonya T. Dyhrman
    Abstract:

    Abstract. N2 fixation by the genus Trichodesmium is predicted to support a large proportion of the primary productivity across the oligotrophic oceans, regions that are considered among the largest biomes on Earth. Many of these environments remain poorly sampled, limiting our understanding of Trichodesmium physiological ecology in these critical oligotrophic regions. Trichodesmium colonies, communities that consisted of the Trichodesmium host and their associated microbiome, were collected across the oligotrophic western tropical South Pacific (WTSP). These samples were used to assess host clade distribution, host and microbiome (holobiont) metabolic potential, and functional gene expression, with a focus on identifying Trichodesmium physiological ecology in this region. Expression dynamics across the WTSP transect indicated potential co-limitation of Trichodesmium for phosphorus and iron. A gene cassette for phosphonate biosynthesis was detected in Trichodesmium, the expression of which co-varied with the abundance of Trichodesmium Clade III, which was unusually abundant relative to Clade I in this environment. Coincident with the expression of the gene cassette, phosphate reduction to phosphite and low molecular weight phosphonate compounds was measured in Trichodesmium colonies as well as genes that enable use of this reduced phosphorus in both Trichodesmium and the microbiome. Overall, these results highlight physiological strategies for survival by the Trichodesmium holobiont in the oligotrophic ocean, revealing mechanisms with the potential to influence the cycling of resources like nitrogen and phosphorus.

  • transcriptional patterns identify resource controls on the diazotroph Trichodesmium in the atlantic and pacific oceans
    The ISME Journal, 2018
    Co-Authors: Sonya T. Dyhrman, Kyle R. Frischkorn, Mónica Rouco, Sheean T. Haley, Harriet Alexander
    Abstract:

    The N2-fixing cyanobacterium Trichodesmium is intensely studied because of the control this organism exerts over the cycling of carbon and nitrogen in the low nutrient ocean gyres. Although iron (Fe) and phosphorus (P) bioavailability are thought to be major drivers of Trichodesmium distributions and activities, identifying resource controls on Trichodesmium is challenging, as Fe and P are often organically complexed and their bioavailability to a single species in a mixed community is difficult to constrain. Further, Fe and P geochemistries are linked through the activities of metalloenzymes, such as the alkaline phosphatases (APs) PhoX and PhoA, which are used by microbes to access dissolved organic P (DOP). Here we identified significant correlations between Trichodesmium-specific transcriptional patterns in the North Atlantic (NASG) and North Pacific Subtropical Gyres (NPSG) and patterns in Fe and P biogeochemistry, with the relative enrichment of Fe stress markers in the NPSG, and P stress markers in the NASG. We also observed the differential enrichment of Fe-requiring PhoX transcripts in the NASG and Fe-insensitive PhoA transcripts in the NPSG, suggesting that metalloenzyme switching may be used to mitigate Fe limitation of DOP metabolism in Trichodesmium. This trait may underpin Trichodesmium success across disparate ecosystems.

  • coordinated gene expression between Trichodesmium and its microbiome over day night cycles in the north pacific subtropical gyre
    The ISME Journal, 2018
    Co-Authors: Sonya T. Dyhrman, Kyle R. Frischkorn, Sheean T. Haley
    Abstract:

    Trichodesmium is a widespread, N2 fixing marine cyanobacterium that drives inputs of newly fixed nitrogen and carbon into the oligotrophic ecosystems where it occurs. Colonies of Trichodesmium ubiquitously occur with heterotrophic bacteria that make up a diverse microbiome, and interactions within this Trichodesmium holobiont could influence the fate of fixed carbon and nitrogen. Metatranscriptome sequencing was performed on Trichodesmium colonies collected during high-frequency Lagrangian sampling in the North Pacific Subtropical Gyre (NPSG) to identify possible interactions between the Trichodesmium host and microbiome over day-night cycles. Here we show significantly coordinated patterns of gene expression between host and microbiome, many of which had significant day-night periodicity. The functions of the co-expressed genes suggested a suite of interactions within the holobiont linked to key resources including nitrogen, carbon, and iron. Evidence of microbiome reliance on Trichodesmium-derived vitamin B12 was also detected in co-expression patterns, highlighting a dependency that could shape holobiont community structure. Collectively, these patterns of expression suggest that biotic interactions could influence colony cycling of resources like nitrogen and vitamin B12, and decouple activities, like N2 fixation, from typical abiotic drivers of Trichodesmium physiological ecology.

  • Trichodesmium physiological ecology and phosphate reduction in the western tropical South Pacific
    Biogeosciences, 2018
    Co-Authors: Kyle R. Frischkorn, Andreas Krupke, Mónica Rouco, Andrés E. Salazar Estrada, Benjamin A. S. Van Mooy, Cécile Guieu, Justine Louis, Sonya T. Dyhrman
    Abstract:

    N 2 fixation by the genus Trichodesmium is predicted to support a large proportion of the primary productivity across the oligotrophic oceans, regions that are considered among the largest biomes on Earth. Many of these environments remain poorly sampled, limiting our understanding of Trichodesmium physiological ecology in these critical oligotrophic regions. Trichodesmium colonies, communities that consist of the Trichodesmium host and their associated microbiome, were collected across the oligotrophic western tropical South Pacific (WTSP). These samples were used to assess host clade distribution, host and microbiome metabolic potential, and functional gene expression, with a focus on identifying Trichodesmium physiological ecology in this region. Genes sets related to phosphorus, iron, and phosphorus-iron co-limitation were dynamically expressed across the WTSP transect, suggestive of the importance of these resources in driving Trichodesmium physiological ecology in this region. A gene cassette for phosphonate biosynthesis was detected in Trichodesmium, the expression of which co-varied with the abundance of Trichodesmium Clade III, which was unusually abundant relative to Clade I in this environment. Coincident with the expression of the gene cassette, phosphate reduction to phosphite and low-molecular-weight phosphonate compounds was measured in Trichodesmium colonies. The expression of genes that enable use of such reduced-phosphorus compounds were also measured in both Trichodesmium and the microbiome. Overall , these results highlight physiological strategies employed by consortia in an undersampled region of the oligotrophic WTSP and reveal the molecular mechanisms underlying previously observed high rates of phosphorus reduction in Tri-chodesmium colonies.

  • Epibionts dominate metabolic functional potential of Trichodesmium colonies from the oligotrophic ocean.
    The ISME Journal, 2017
    Co-Authors: Kyle R. Frischkorn, Mónica Rouco, Benjamin A. S. Van Mooy, Sonya T. Dyhrman
    Abstract:

    Trichodesmium is a genus of marine diazotrophic colonial cyanobacteria that exerts a profound influence on global biogeochemistry, by injecting ‘new’ nitrogen into the low nutrient systems where it occurs. Colonies of Trichodesmium ubiquitously contain a diverse assemblage of epibiotic microorganisms, constituting a microbiome on the Trichodesmium host. Metagenome sequences from Trichodesmium colonies were analyzed along a resource gradient in the western North Atlantic to examine microbiome community structure, functional diversity and metabolic contributions to the holobiont. Here we demonstrate the presence of a core Trichodesmium microbiome that is modulated to suit different ocean regions, and contributes over 10 times the metabolic potential of Trichodesmium to the holobiont. Given the ubiquitous nature of epibionts on colonies, the substantial functional diversity within the microbiome is likely an integral facet of Trichodesmium physiological ecology across the oligotrophic oceans where this biogeochemically significant diazotroph thrives.

Douglas G Capone - One of the best experts on this subject based on the ideXlab platform.

  • fixation and fate of c and n in the cyanobacterium Trichodesmium using nanometer scale secondary ion mass spectrometry
    Proceedings of the National Academy of Sciences of the United States of America, 2009
    Co-Authors: Juliette A Finzihart, Jennifer Pettridge, Peter K Weber, Radu Popa, Stewart Fallon, Troy Gunderson, I D Hutcheon, Kenneth H Nealson, Douglas G Capone
    Abstract:

    The marine cyanobacterium Trichodesmium is ubiquitous in tropical and subtropical seas and is an important contributor to global N and C cycling. We sought to characterize metabolic uptake patterns in individual Trichodesmium IMS-101 cells by quantitatively imaging 13C and 15N uptake with high-resolution secondary ion mass spectrometry (NanoSIMS). Trichodesmium fix both CO2 and N2 concurrently during the day and are, thus, faced with a balancing act: the O2 evolved during photosynthesis inhibits nitrogenase, the key enzyme in N2 fixation. After performing correlated transmission electron microscopy (TEM) and NanoSIMS analysis on trichome thin-sections, we observed transient inclusion of 15N and 13C into discrete subcellular bodies identified as cyanophycin granules. We speculate that Trichodesmium uses these dynamic storage bodies to uncouple CO2 and N2 fixation from overall growth dynamics. We also directly quantified both CO2 and N2 fixation at the single cell level using NanoSIMS imaging of whole cells in multiple trichomes. Our results indicate maximal CO2 fixation rates in the morning, compared with maximal N2 fixation rates in the afternoon, bolstering the argument that segregation of CO2 and N2 fixation in Trichodesmium is regulated in part by temporal factors. Spatial separation of N2 and CO2 fixation may also have a role in metabolic segregation in Trichodesmium. Our approach in combining stable isotope labeling with NanoSIMS and TEM imaging can be extended to other physiologically relevant elements and processes in other important microbial systems.

  • fixation and fate of c and n in the cyanobacterium Trichodesmium using nanometer scale secondary ion mass spectrometry
    Proceedings of the National Academy of Sciences of the United States of America, 2009
    Co-Authors: Juliette A Finzihart, Jennifer Pettridge, Peter K Weber, Radu Popa, Stewart Fallon, Troy Gunderson, I D Hutcheon, Kenneth H Nealson, Douglas G Capone
    Abstract:

    The marine cyanobacterium Trichodesmium is ubiquitous in tropical and subtropical seas and is an important contributor to global N and C cycling. We sought to characterize metabolic uptake patterns in individual Trichodesmium IMS-101 cells by quantitatively imaging 13C and 15N uptake with high-resolution secondary ion mass spectrometry (NanoSIMS). Trichodesmium fix both CO2 and N2 concurrently during the day and are, thus, faced with a balancing act: the O2 evolved during photosynthesis inhibits nitrogenase, the key enzyme in N2 fixation. After performing correlated transmission electron microscopy (TEM) and NanoSIMS analysis on trichome thin-sections, we observed transient inclusion of 15N and 13C into discrete subcellular bodies identified as cyanophycin granules. We speculate that Trichodesmium uses these dynamic storage bodies to uncouple CO2 and N2 fixation from overall growth dynamics. We also directly quantified both CO2 and N2 fixation at the single cell level using NanoSIMS imaging of whole cells in multiple trichomes. Our results indicate maximal CO2 fixation rates in the morning, compared with maximal N2 fixation rates in the afternoon, bolstering the argument that segregation of CO2 and N2 fixation in Trichodesmium is regulated in part by temporal factors. Spatial separation of N2 and CO2 fixation may also have a role in metabolic segregation in Trichodesmium. Our approach in combining stable isotope labeling with NanoSIMS and TEM imaging can be extended to other physiologically relevant elements and processes in other important microbial systems.

  • Phosphorus dynamics of the tropical and subtropical north Atlantic : Trichodesmium spp. versus bulk plankton
    Marine Ecology Progress Series, 2006
    Co-Authors: Jill A. Sohm, Douglas G Capone
    Abstract:

    Nitrogen fixing organisms such as Trichodesmium spp. are abundant in the oligotrophic tropical North Atlantic Ocean, where microplankton (including other diazotrophs) are more likely to be phosphorus (P) than nitrogen (N) limited. Thus, understanding the ability of different functional groups in the plankton to compete for P in this area is important for understanding their relative success. The uptake of phosphate by Trichodesmium spp. colonies and bulk water plankton was measured using 33 PO4 3- over a range of concentrations, and kinetic parameters were determined. Nano- and pico-plankton present in bulk water samples have a Ks that is nearly 30 times lower than that of Trichodesmium spp. While chl a-normalized alkaline phosphatase activity (APA) in bulk water was an order of magnitude greater than in Trichodesmium spp., Trichodesmium spp. contributes sub- stantially to total APA in the water. Trichodesmium spp. is outcompeted for dissolved inorganic P (DIP), but colonies can satisfy their P needs by supplementing DIP uptake with P cleaved from dissolved organic P (DOP) via alkaline phosphatase.

  • nitrogen fixation by Trichodesmium spp an important source of new nitrogen to the tropical and subtropical north atlantic ocean
    Global Biogeochemical Cycles, 2005
    Co-Authors: Douglas G Capone, James A Burns, Ajit Subramaniam, Claire Mahaffey, Joseph P Montoya, Troy Gunderson, Anthony F Michaels, Edward J. Carpenter
    Abstract:

    [1] The broad distribution and often high densities of the cyanobacterium Trichodesmium spp. in oligotrophic waters imply a substantial role for this one taxon in the oceanic N cycle of the marine tropics and subtropics. New results from 154 stations on six research cruises in the North Atlantic Ocean show depth-integrated N2 fixation by Trichodesmium spp. at many stations that equalled or exceeded the estimated vertical flux of NO3− into the euphotic zone by diapycnal mixing. Areal rates are consistent with those derived from several indirect geochemical analyses. Direct measurements of N2 fixation rates by Trichodesmium are also congruent with upper water column N budgets derived from parallel determinations of stable isotope distributions, clearly showing that N2 fixation by Trichodesmium is a major source of new nitrogen in the tropical North Atlantic. We project a conservative estimate of the annual input of new N into the tropical North Atlantic of at least 1.6 × 1012 mol N by Trichodesmium N2 fixation alone. This input can account for a substantial fraction of the N2 fixation in the North Atlantic inferred by several of the geochemical approaches.

  • biomass and primary productivity of the cyanobacterium Trichodesmium spp in the tropical n atlantic ocean
    Deep Sea Research Part I: Oceanographic Research Papers, 2004
    Co-Authors: Edward J. Carpenter, Ajit Subramaniam, Douglas G Capone
    Abstract:

    Abstract Primary production and standing crop, as chlorophyll- a (chl- a ), of Trichodesmium spp., and other phytoplankton as well as the abundance and depth distribution of Trichodesmium were measured on three cruises to the tropical North Atlantic Ocean. Trichodesmium abundance was greatest on a cruise in May–June 1994, with average surface densities of 2250 trichomes l −1 and depth integrated abundance of 91×10 6  trichomes m −2 . Average surface densities were 292 and 222 trichomes l −1 and depth integrated abundance 21 and 8.6×10 6  trichomes m −2 for the April 1996 and October 1996 cruises, respectively. Total (phytoplankton plus Trichodesmium ) chl- a standing crop and the percentage as Trichodesmium averaged 47 (62%), 22 (13%) and 30 (11%) mg chl- a  m −2 for May–June 1994 and April and October 1996. On the May–June 1994 and April and October 1996 cruises 89%, 93% and 92% of the trichomes were in colonies, and the remainder occurred as free trichomes. Peak abundances of Trichodesmium were generally in the upper water column, with an average biomass maximum at 12 m on the May–June 94 and October 96 cruises and at 40 m during the April 96 cruise. The average C:N ratio (atomic) of Trichodesmium was 6.5. Mean rates of total primary production ( Trichodesmium and other phytoplankton together) for May–June 1994, and April and October 1996 were 1080, 932 and 804 mg C m −2  d −1 , and Trichodesmium accounted for an average of 47%, 7.9% and 11%, respectively, of the total primary production for each cruise. These primary production rates exceed those typically reported at oligotrophic open ocean sites. Trichodesmium C assimilation numbers (mg C fixed mg chl- a −1  h −1 ) were highest at the surface and were always lower than those of other phytoplankton. Average nitrogen demand, as calculated from the mean Trichodesmium C fixation from all three cruises, was about 40 mg N m −2  d −1 , about 10% of concurrently determined rates of N 2 fixation.

Edward J. Carpenter - One of the best experts on this subject based on the ideXlab platform.

  • Association of the copepod Macrosetella gracilis with the cyanobacterium Trichodesmium spp. in the North Pacific Gyre
    Marine Ecology Progress Series, 2007
    Co-Authors: Renate Eberl, Edward J. Carpenter
    Abstract:

    The harpacticoid copepod Macrosetella gracilis is found in pelagic habitats in tropical and subtropical oceans associated with colonies of the N2 fixing cyanobacterium Trichodesmium spp. In the central North Pacific near Hawaii, M. gracilis was abundant (1.8 ± 1.4 (SD) M. gracilis adults m -3 and 4.7 ± 3.9 M. gracilis copepodites m -3 ) and constituted an average of 10.8% of the total copepod population. However, we observed no statistically discernable correlation between M. gracilis and Trichodesmium spp. abundances, suggesting that availability of Trichodesmium spp. did not limit the abundance of M. gracilis during our study. In previous laboratory studies M. gracilis had been shown to have the ability to ingest Trichodesmium spp. trichomes and appeared immune to cyano- bacterial toxins harmful to other species of copepods. Natural abundance of stable isotopes (δ 15 N, δ 13 C) in copepod tissue from field samples suggested that the diet of M. gracilis was not predominately composed of Trichodesmium spp. as proposed by previous research. Natural abundance of δ 15 N was similar for M. gracilis (3.06 ± 2.29), Miracia efferata (1.83 ± 0.88), and calanoid copepods (2.7 ± 1.95). No Trichodesmium spp. were observed in M. gracilis gut contents. Trichodesmium spp. was not a predominant food in the diet of this copepod, but colonies of the toxic cyanobacterium could provide shelter from predation and be used as a floating substrate for adult and juveniles of M. gracilis.

  • nitrogen fixation by Trichodesmium spp an important source of new nitrogen to the tropical and subtropical north atlantic ocean
    Global Biogeochemical Cycles, 2005
    Co-Authors: Douglas G Capone, James A Burns, Ajit Subramaniam, Claire Mahaffey, Joseph P Montoya, Troy Gunderson, Anthony F Michaels, Edward J. Carpenter
    Abstract:

    [1] The broad distribution and often high densities of the cyanobacterium Trichodesmium spp. in oligotrophic waters imply a substantial role for this one taxon in the oceanic N cycle of the marine tropics and subtropics. New results from 154 stations on six research cruises in the North Atlantic Ocean show depth-integrated N2 fixation by Trichodesmium spp. at many stations that equalled or exceeded the estimated vertical flux of NO3− into the euphotic zone by diapycnal mixing. Areal rates are consistent with those derived from several indirect geochemical analyses. Direct measurements of N2 fixation rates by Trichodesmium are also congruent with upper water column N budgets derived from parallel determinations of stable isotope distributions, clearly showing that N2 fixation by Trichodesmium is a major source of new nitrogen in the tropical North Atlantic. We project a conservative estimate of the annual input of new N into the tropical North Atlantic of at least 1.6 × 1012 mol N by Trichodesmium N2 fixation alone. This input can account for a substantial fraction of the N2 fixation in the North Atlantic inferred by several of the geochemical approaches.

  • biomass and primary productivity of the cyanobacterium Trichodesmium spp in the tropical n atlantic ocean
    Deep Sea Research Part I: Oceanographic Research Papers, 2004
    Co-Authors: Edward J. Carpenter, Ajit Subramaniam, Douglas G Capone
    Abstract:

    Abstract Primary production and standing crop, as chlorophyll- a (chl- a ), of Trichodesmium spp., and other phytoplankton as well as the abundance and depth distribution of Trichodesmium were measured on three cruises to the tropical North Atlantic Ocean. Trichodesmium abundance was greatest on a cruise in May–June 1994, with average surface densities of 2250 trichomes l −1 and depth integrated abundance of 91×10 6  trichomes m −2 . Average surface densities were 292 and 222 trichomes l −1 and depth integrated abundance 21 and 8.6×10 6  trichomes m −2 for the April 1996 and October 1996 cruises, respectively. Total (phytoplankton plus Trichodesmium ) chl- a standing crop and the percentage as Trichodesmium averaged 47 (62%), 22 (13%) and 30 (11%) mg chl- a  m −2 for May–June 1994 and April and October 1996. On the May–June 1994 and April and October 1996 cruises 89%, 93% and 92% of the trichomes were in colonies, and the remainder occurred as free trichomes. Peak abundances of Trichodesmium were generally in the upper water column, with an average biomass maximum at 12 m on the May–June 94 and October 96 cruises and at 40 m during the April 96 cruise. The average C:N ratio (atomic) of Trichodesmium was 6.5. Mean rates of total primary production ( Trichodesmium and other phytoplankton together) for May–June 1994, and April and October 1996 were 1080, 932 and 804 mg C m −2  d −1 , and Trichodesmium accounted for an average of 47%, 7.9% and 11%, respectively, of the total primary production for each cruise. These primary production rates exceed those typically reported at oligotrophic open ocean sites. Trichodesmium C assimilation numbers (mg C fixed mg chl- a −1  h −1 ) were highest at the surface and were always lower than those of other phytoplankton. Average nitrogen demand, as calculated from the mean Trichodesmium C fixation from all three cruises, was about 40 mg N m −2  d −1 , about 10% of concurrently determined rates of N 2 fixation.

  • Detecting Trichodesmium blooms in SeaWiFS imagery
    Deep-sea Research Part Ii-topical Studies in Oceanography, 2001
    Co-Authors: Ajit Subramaniam, Edward J. Carpenter, Chris W. Brown, Raleigh R. Hood, Douglas G Capone
    Abstract:

    A multispectral classification scheme was developed to detect the cyanobacteria Trichodesmium spp. in satellite data of the sea-viewing wide field-of-view sensor (SeaWiFS). The criteria for this scheme were established from spectral characteristics derived from (1) SeaWiFS imagery of a Trichodesmium bloom located in the South Atlantic Bight and (2) modeled remote sensing reflectances of Trichodesmium and other phytoplankton. The classification scheme, which is valid for moderate chlorophyll concentrations of Trichodesmium in coastal waters, is based on the magnitude of the 490-channel reflectance and the spectral shape of remote sensing reflectance at 443, 490 and 555 nm. Analysis suggests that the spatial structure of Trichodesmium populations at sub-pixel scales must be considered when employing spectral characteristics to detect their presence in satellite imagery. This study demonstrates the potential of mapping Trichodesmium from space using spectral observations, even in waters as optically complex as the South Atlantic Bight. Future efforts, which will incorporate ancillary data such as wind speeds and water temperature, will improve the likelihood of correct identification.

  • Remote estimation of nitrogen fixation by Trichodesmium
    Deep-sea Research Part Ii-topical Studies in Oceanography, 2001
    Co-Authors: Raleigh R. Hood, Edward J. Carpenter, Ajit Subramaniam, Linda R. May, Douglas G Capone
    Abstract:

    Abstract A non-spectral model is described that can be used to calculate N 2 -fixation rate from remote estimates of Trichodesmium biomass. This model, which is similar to formulations that have been developed for estimating primary production from satellite-derived phytoplankton chlorophyll concentrations, is parameterized using measured Trichodesmium N 2 -fixation vs. irradiance ( I ) data and observed subsurface Trichodesmium biomass profiles from the Tropical Atlantic Ocean. These data reveal that the N 2 -fixation vs. I responses and subsurface distributions of Trichodesmium vary substantially in tropical waters. The calculated rates are sensitive to only one of three forcing variables: the remotely sensed Trichodesmium chlorophyll concentration, B T sat , and two of the model parameters: the maximum N 2 -fixation rate, P max B T , and the depth of the subsurface Trichodesmium biomass maximum, Z m . The model is particularly sensitive to the latter. These results suggest that in order to generate N 2 -fixation rate estimates with reasonable confidence limits with this model, means must be sought to account for in situ variablity in P max B T and Z m . A series of correlation analyses reveal statistically significant correlations between the diffuse attenuation coefficient, K par , and P max B T , and between wind speed and Z m . These relationships are suggested as potential means of accounting for natural variability in P max B T and Z m . An example remote sensing-based rate calculation is made using SeaWiFS-derived Trichodesmium chlorophyll concentration in the South Atlantic Bight described in Subramaniam et al., 2002 (Deep-Sea Research, 2002). Although the optical conditions in the Bight were not all within the range used to derive the model parameters, the model gives rates that are consistent with direct rate measurements in Trichodesmium blooms. Because Trichodesmium biomass can only be detected remotely at relatively high concentrations, efforts to estimate global rates with this model will require the use of both shipboard and satellite data.

Kyle R. Frischkorn - One of the best experts on this subject based on the ideXlab platform.

  • <i>Trichodesmium</i> physiological ecology and phosphate reduction in the western Tropical South Pacific
    2018
    Co-Authors: Kyle R. Frischkorn, Andreas Krupke, Mónica Rouco, Andrés E. Salazar Estrada, Benjamin A. S. Van Mooy, Sonya T. Dyhrman
    Abstract:

    Abstract. N2 fixation by the genus Trichodesmium is predicted to support a large proportion of the primary productivity across the oligotrophic oceans, regions that are considered among the largest biomes on Earth. Many of these environments remain poorly sampled, limiting our understanding of Trichodesmium physiological ecology in these critical oligotrophic regions. Trichodesmium colonies, communities that consisted of the Trichodesmium host and their associated microbiome, were collected across the oligotrophic western tropical South Pacific (WTSP). These samples were used to assess host clade distribution, host and microbiome (holobiont) metabolic potential, and functional gene expression, with a focus on identifying Trichodesmium physiological ecology in this region. Expression dynamics across the WTSP transect indicated potential co-limitation of Trichodesmium for phosphorus and iron. A gene cassette for phosphonate biosynthesis was detected in Trichodesmium, the expression of which co-varied with the abundance of Trichodesmium Clade III, which was unusually abundant relative to Clade I in this environment. Coincident with the expression of the gene cassette, phosphate reduction to phosphite and low molecular weight phosphonate compounds was measured in Trichodesmium colonies as well as genes that enable use of this reduced phosphorus in both Trichodesmium and the microbiome. Overall, these results highlight physiological strategies for survival by the Trichodesmium holobiont in the oligotrophic ocean, revealing mechanisms with the potential to influence the cycling of resources like nitrogen and phosphorus.

  • transcriptional patterns identify resource controls on the diazotroph Trichodesmium in the atlantic and pacific oceans
    The ISME Journal, 2018
    Co-Authors: Sonya T. Dyhrman, Kyle R. Frischkorn, Mónica Rouco, Sheean T. Haley, Harriet Alexander
    Abstract:

    The N2-fixing cyanobacterium Trichodesmium is intensely studied because of the control this organism exerts over the cycling of carbon and nitrogen in the low nutrient ocean gyres. Although iron (Fe) and phosphorus (P) bioavailability are thought to be major drivers of Trichodesmium distributions and activities, identifying resource controls on Trichodesmium is challenging, as Fe and P are often organically complexed and their bioavailability to a single species in a mixed community is difficult to constrain. Further, Fe and P geochemistries are linked through the activities of metalloenzymes, such as the alkaline phosphatases (APs) PhoX and PhoA, which are used by microbes to access dissolved organic P (DOP). Here we identified significant correlations between Trichodesmium-specific transcriptional patterns in the North Atlantic (NASG) and North Pacific Subtropical Gyres (NPSG) and patterns in Fe and P biogeochemistry, with the relative enrichment of Fe stress markers in the NPSG, and P stress markers in the NASG. We also observed the differential enrichment of Fe-requiring PhoX transcripts in the NASG and Fe-insensitive PhoA transcripts in the NPSG, suggesting that metalloenzyme switching may be used to mitigate Fe limitation of DOP metabolism in Trichodesmium. This trait may underpin Trichodesmium success across disparate ecosystems.

  • coordinated gene expression between Trichodesmium and its microbiome over day night cycles in the north pacific subtropical gyre
    The ISME Journal, 2018
    Co-Authors: Sonya T. Dyhrman, Kyle R. Frischkorn, Sheean T. Haley
    Abstract:

    Trichodesmium is a widespread, N2 fixing marine cyanobacterium that drives inputs of newly fixed nitrogen and carbon into the oligotrophic ecosystems where it occurs. Colonies of Trichodesmium ubiquitously occur with heterotrophic bacteria that make up a diverse microbiome, and interactions within this Trichodesmium holobiont could influence the fate of fixed carbon and nitrogen. Metatranscriptome sequencing was performed on Trichodesmium colonies collected during high-frequency Lagrangian sampling in the North Pacific Subtropical Gyre (NPSG) to identify possible interactions between the Trichodesmium host and microbiome over day-night cycles. Here we show significantly coordinated patterns of gene expression between host and microbiome, many of which had significant day-night periodicity. The functions of the co-expressed genes suggested a suite of interactions within the holobiont linked to key resources including nitrogen, carbon, and iron. Evidence of microbiome reliance on Trichodesmium-derived vitamin B12 was also detected in co-expression patterns, highlighting a dependency that could shape holobiont community structure. Collectively, these patterns of expression suggest that biotic interactions could influence colony cycling of resources like nitrogen and vitamin B12, and decouple activities, like N2 fixation, from typical abiotic drivers of Trichodesmium physiological ecology.

  • Trichodesmium physiological ecology and phosphate reduction in the western tropical South Pacific
    Biogeosciences, 2018
    Co-Authors: Kyle R. Frischkorn, Andreas Krupke, Mónica Rouco, Andrés E. Salazar Estrada, Benjamin A. S. Van Mooy, Cécile Guieu, Justine Louis, Sonya T. Dyhrman
    Abstract:

    N 2 fixation by the genus Trichodesmium is predicted to support a large proportion of the primary productivity across the oligotrophic oceans, regions that are considered among the largest biomes on Earth. Many of these environments remain poorly sampled, limiting our understanding of Trichodesmium physiological ecology in these critical oligotrophic regions. Trichodesmium colonies, communities that consist of the Trichodesmium host and their associated microbiome, were collected across the oligotrophic western tropical South Pacific (WTSP). These samples were used to assess host clade distribution, host and microbiome metabolic potential, and functional gene expression, with a focus on identifying Trichodesmium physiological ecology in this region. Genes sets related to phosphorus, iron, and phosphorus-iron co-limitation were dynamically expressed across the WTSP transect, suggestive of the importance of these resources in driving Trichodesmium physiological ecology in this region. A gene cassette for phosphonate biosynthesis was detected in Trichodesmium, the expression of which co-varied with the abundance of Trichodesmium Clade III, which was unusually abundant relative to Clade I in this environment. Coincident with the expression of the gene cassette, phosphate reduction to phosphite and low-molecular-weight phosphonate compounds was measured in Trichodesmium colonies. The expression of genes that enable use of such reduced-phosphorus compounds were also measured in both Trichodesmium and the microbiome. Overall , these results highlight physiological strategies employed by consortia in an undersampled region of the oligotrophic WTSP and reveal the molecular mechanisms underlying previously observed high rates of phosphorus reduction in Tri-chodesmium colonies.

  • Epibionts dominate metabolic functional potential of Trichodesmium colonies from the oligotrophic ocean.
    The ISME Journal, 2017
    Co-Authors: Kyle R. Frischkorn, Mónica Rouco, Benjamin A. S. Van Mooy, Sonya T. Dyhrman
    Abstract:

    Trichodesmium is a genus of marine diazotrophic colonial cyanobacteria that exerts a profound influence on global biogeochemistry, by injecting ‘new’ nitrogen into the low nutrient systems where it occurs. Colonies of Trichodesmium ubiquitously contain a diverse assemblage of epibiotic microorganisms, constituting a microbiome on the Trichodesmium host. Metagenome sequences from Trichodesmium colonies were analyzed along a resource gradient in the western North Atlantic to examine microbiome community structure, functional diversity and metabolic contributions to the holobiont. Here we demonstrate the presence of a core Trichodesmium microbiome that is modulated to suit different ocean regions, and contributes over 10 times the metabolic potential of Trichodesmium to the holobiont. Given the ubiquitous nature of epibionts on colonies, the substantial functional diversity within the microbiome is likely an integral facet of Trichodesmium physiological ecology across the oligotrophic oceans where this biogeochemically significant diazotroph thrives.

Troy Gunderson - One of the best experts on this subject based on the ideXlab platform.

  • fixation and fate of c and n in the cyanobacterium Trichodesmium using nanometer scale secondary ion mass spectrometry
    Proceedings of the National Academy of Sciences of the United States of America, 2009
    Co-Authors: Juliette A Finzihart, Jennifer Pettridge, Peter K Weber, Radu Popa, Stewart Fallon, Troy Gunderson, I D Hutcheon, Kenneth H Nealson, Douglas G Capone
    Abstract:

    The marine cyanobacterium Trichodesmium is ubiquitous in tropical and subtropical seas and is an important contributor to global N and C cycling. We sought to characterize metabolic uptake patterns in individual Trichodesmium IMS-101 cells by quantitatively imaging 13C and 15N uptake with high-resolution secondary ion mass spectrometry (NanoSIMS). Trichodesmium fix both CO2 and N2 concurrently during the day and are, thus, faced with a balancing act: the O2 evolved during photosynthesis inhibits nitrogenase, the key enzyme in N2 fixation. After performing correlated transmission electron microscopy (TEM) and NanoSIMS analysis on trichome thin-sections, we observed transient inclusion of 15N and 13C into discrete subcellular bodies identified as cyanophycin granules. We speculate that Trichodesmium uses these dynamic storage bodies to uncouple CO2 and N2 fixation from overall growth dynamics. We also directly quantified both CO2 and N2 fixation at the single cell level using NanoSIMS imaging of whole cells in multiple trichomes. Our results indicate maximal CO2 fixation rates in the morning, compared with maximal N2 fixation rates in the afternoon, bolstering the argument that segregation of CO2 and N2 fixation in Trichodesmium is regulated in part by temporal factors. Spatial separation of N2 and CO2 fixation may also have a role in metabolic segregation in Trichodesmium. Our approach in combining stable isotope labeling with NanoSIMS and TEM imaging can be extended to other physiologically relevant elements and processes in other important microbial systems.

  • fixation and fate of c and n in the cyanobacterium Trichodesmium using nanometer scale secondary ion mass spectrometry
    Proceedings of the National Academy of Sciences of the United States of America, 2009
    Co-Authors: Juliette A Finzihart, Jennifer Pettridge, Peter K Weber, Radu Popa, Stewart Fallon, Troy Gunderson, I D Hutcheon, Kenneth H Nealson, Douglas G Capone
    Abstract:

    The marine cyanobacterium Trichodesmium is ubiquitous in tropical and subtropical seas and is an important contributor to global N and C cycling. We sought to characterize metabolic uptake patterns in individual Trichodesmium IMS-101 cells by quantitatively imaging 13C and 15N uptake with high-resolution secondary ion mass spectrometry (NanoSIMS). Trichodesmium fix both CO2 and N2 concurrently during the day and are, thus, faced with a balancing act: the O2 evolved during photosynthesis inhibits nitrogenase, the key enzyme in N2 fixation. After performing correlated transmission electron microscopy (TEM) and NanoSIMS analysis on trichome thin-sections, we observed transient inclusion of 15N and 13C into discrete subcellular bodies identified as cyanophycin granules. We speculate that Trichodesmium uses these dynamic storage bodies to uncouple CO2 and N2 fixation from overall growth dynamics. We also directly quantified both CO2 and N2 fixation at the single cell level using NanoSIMS imaging of whole cells in multiple trichomes. Our results indicate maximal CO2 fixation rates in the morning, compared with maximal N2 fixation rates in the afternoon, bolstering the argument that segregation of CO2 and N2 fixation in Trichodesmium is regulated in part by temporal factors. Spatial separation of N2 and CO2 fixation may also have a role in metabolic segregation in Trichodesmium. Our approach in combining stable isotope labeling with NanoSIMS and TEM imaging can be extended to other physiologically relevant elements and processes in other important microbial systems.

  • nitrogen fixation by Trichodesmium spp an important source of new nitrogen to the tropical and subtropical north atlantic ocean
    Global Biogeochemical Cycles, 2005
    Co-Authors: Douglas G Capone, James A Burns, Ajit Subramaniam, Claire Mahaffey, Joseph P Montoya, Troy Gunderson, Anthony F Michaels, Edward J. Carpenter
    Abstract:

    [1] The broad distribution and often high densities of the cyanobacterium Trichodesmium spp. in oligotrophic waters imply a substantial role for this one taxon in the oceanic N cycle of the marine tropics and subtropics. New results from 154 stations on six research cruises in the North Atlantic Ocean show depth-integrated N2 fixation by Trichodesmium spp. at many stations that equalled or exceeded the estimated vertical flux of NO3− into the euphotic zone by diapycnal mixing. Areal rates are consistent with those derived from several indirect geochemical analyses. Direct measurements of N2 fixation rates by Trichodesmium are also congruent with upper water column N budgets derived from parallel determinations of stable isotope distributions, clearly showing that N2 fixation by Trichodesmium is a major source of new nitrogen in the tropical North Atlantic. We project a conservative estimate of the annual input of new N into the tropical North Atlantic of at least 1.6 × 1012 mol N by Trichodesmium N2 fixation alone. This input can account for a substantial fraction of the N2 fixation in the North Atlantic inferred by several of the geochemical approaches.