scholarly journals Dissolved organic matter stimulates N2 fixation and nifH gene expression in Trichodesmium

2020 ◽  
Vol 367 (4) ◽  
Author(s):  
Mar Benavides ◽  
Solange Duhamel ◽  
France Van Wambeke ◽  
Katyanne M Shoemaker ◽  
Pia H Moisander ◽  
...  

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.

2008 ◽  
Vol 5 (2) ◽  
pp. 281-298 ◽  
Author(s):  
P. Raimbault ◽  
N. Garcia ◽  
F. Cerutti

Abstract. During the BIOSOPE cruise the RV Atalante was dedicated to study the biogeochemical properties in the South Pacific between the Marquesas Islands (141° W–8° S) and the Chilean upwelling (73° W–34° S). Over the 8000 km covered by the cruise, several different trophic situations were encountered, in particular strong oligotrophic conditions in the South Pacific Gyre (SPG, between 123° W and 101° W). In this isolated region, nitrate was undetectable between the surface and 160–180 m and only trace quantities (<20 nmoles l−1) of regenerated nitrogen (nitrite and ammonium) were detected, even in the subsurface maximum. Integrated nitrate over the photic layer, which reached 165 m, was close to zero. Despite this severe nitrogen-depletion, phosphate was always present in significant concentrations (≈0.1 μmoles l−1), while silicic acid was maintained at low but classical oceanic levels (≈1 μmoles l−1). In contrast, the Marquesas region (MAR) to the west and Chilean upwelling (UPW) to the east were characterized by high nutrient concentrations, one hundred to one thousand fold higher than in the SPG. The distribution of surface chlorophyll reflected the nitrate gradient, the lowest concentrations (0.023 nmoles l−1) being measured at the centre of the SPG, where integrated value throughout the photic layer was very low (≈ 10 mg m−2). However, due to the relatively high concentrations of chlorophyll-a encountered in the DCM (0.2 μg l−1), chlorophyll-a concentrations throughout the photic layer were less variable than nitrate concentrations (by a factor 2 to 5). In contrast to chlorophyll-a, integrated particulate organic matter (POM) remained more or less constant along the study area (500 mmoles m−2, 60 mmoles m−2 and 3.5 mmoles m−2 for particulate organic carbon, particulate organic nitrogen and particulate organic phosphorus, respectively), with the exception of the upwelling, where values were two fold higher. The residence time of particulate carbon in the surface water was only 4–5 days in the upwelling, but up to 30 days in the SPG, where light isotopic δ15N signal noted in the suspended POM suggests that N2-fixation provides a dominant supply of nitrogen to phytoplankton. The most striking feature was the large accumulation of dissolved organic matter (DOM) in the SPG compared to the surrounding waters, in particular dissolved organic carbon (DOC) where concentrations were at levels rarely measured in oceanic waters (>100 μmoles l−1). Due to this large pool of DOM in the SPG photic layer, integrated values followed a converse geographical pattern to that of inorganic nutrients with a large accumulation in the centre of the SPG. Whereas suspended particulate matter in the mixed layer had a C/N ratio largely conforming to the Redfield stochiometry (C/N≈6.6), marked deviations were observed in this excess DOM (C/N≈16 to 23). The marked geographical trend suggests that a net in situ source exists, mainly due to biological processes. Thus, in spite of strong nitrate-depletion leading to low chlorophyll biomass, the closed ecosystem of the SPG can accumulate large amounts of C-rich dissolved organic matter. The implications of this finding are examined, the conclusion being that, due to weak lateral advection, the biologically produced dissolved organic carbon can be accumulated and stored in the photic layer for very long periods. In spite of the lack of seasonal vertical mixing, a significant part of new production (up to 34%), which was mainly supported by dinitrogen fixation, can be exported to deep waters by turbulent diffusion in terms of DOC. The diffusive rate estimated in the SPG (134 μmolesC m−2 d−1), was quite equivalent to the particles flux measured by sediments traps.


2018 ◽  
Vol 5 ◽  
Author(s):  
Mar Benavides ◽  
Chloé Martias ◽  
Hila Elifantz ◽  
Ilana Berman-Frank ◽  
Cécile Dupouy ◽  
...  

2018 ◽  
Author(s):  
Kyle R. Frischkorn ◽  
Andreas Krupke ◽  
Mónica Rouco ◽  
Andrés E. Salazar Estrada ◽  
Benjamin A. S. Van Mooy ◽  
...  

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.


2015 ◽  
Vol 82 (5) ◽  
pp. 1423-1432 ◽  
Author(s):  
Vincent J. Denef ◽  
Ryan S. Mueller ◽  
Edna Chiang ◽  
James R. Liebig ◽  
Henry A. Vanderploeg

ABSTRACTTheChloroflexiCL500-11 clade contributes a large proportion of the bacterial biomass in the oxygenated hypolimnia of deep lakes worldwide, including the world's largest freshwater system, the Laurentian Great Lakes. Traits that allow CL500-11 to thrive and its biogeochemical role in these environments are currently unknown. Here, we found that a CL500-11 population was present mostly in offshore waters along a transect in ultraoligotrophic Lake Michigan (a Laurentian Great Lake). It occurred throughout the water column in spring and only in the hypolimnion during summer stratification, contributing up to 18.1% of all cells. Genome reconstruction from metagenomic data suggested an aerobic, motile, heterotrophic lifestyle, with additional energy being gained through carboxidovory and methylovory. Comparisons to other available streamlined freshwater genomes revealed that the CL500-11 genome contained a disproportionate number of cell wall/capsule biosynthesis genes and the most diverse spectrum of genes involved in the uptake of dissolved organic matter (DOM) substrates, particularly peptides.In situexpression patterns indicated the importance of DOM uptake and protein/peptide turnover, as well as type I and type II carbon monoxide dehydrogenase and flagellar motility. Its location in the water column influenced its gene expression patterns the most. We observed increased bacteriorhodopsin gene expression and a response to oxidative stress in surface waters compared to its response in deep waters. While CL500-11 carries multiple adaptations to an oligotrophic lifestyle, its investment in motility, its large cell size, and its distribution in both oligotrophic and mesotrophic lakes indicate its ability to thrive under conditions where resources are more plentiful. Our data indicate that CL500-11 plays an important role in nitrogen-rich DOM mineralization in the extensive deep-lake hypolimnion habitat.


1969 ◽  
Vol 49 (3) ◽  
pp. 365-373 ◽  
Author(s):  
M. Lévesque

Fulvic acid–metal–phosphate complexes prepared in the laboratory and corresponding complexes extracted (0.1 N NaOH and chelating resin) from a soil were characterized by means of electrophoresis, Sephadex gel filtration, and methods for differentiation of organic and inorganic phosphorus. The findings can be summarized as follows:(1) The prepared material in aqueous solution (after purification by dialysis) comprised three different entities: a fulvic acid–metal–phosphate complex, a fulvic acid–metal complex, and unbonded inorganic phosphate. These entities were reaction products obtained during the formation of fulvic acid–metal–phosphate complexes.(2) Upon hydrolysis in mild alkaline media, the metal–phosphate bonds of the fulvic acid–metal–phosphate complexes were broken; the fulvic acid–metal complexes, freed from the phosphate, remained intact.(3) While metal ions were necessary for bridging phosphorus and fulvic acid, phosphorus in turn may have bridged the fulvic acid–metal units.(4) Significant amounts of complexed inorganic phosphorus were found intermixed with organic phosphorus compounds in soil extracts; this suggested the existence of organic matter metal–phosphate complexes in soil.


2007 ◽  
Vol 4 (4) ◽  
pp. 3041-3087 ◽  
Author(s):  
P. Raimbault ◽  
N. Garcia ◽  
F. Cerutti

Abstract. The BIOSOPE cruise of the RV Atalante was devoted to study the biogeochemical properties in the South Pacific between the Marquesas Islands (141° W–8° S) and the Chilean upwelling (73° W–34° S). The 8000 km cruise had the opportunity to encounter different trophic situations, and especially strong oligotrophic conditions in the Central South Pacific Gyre (SPG, between 123° W and 101° W). In this isolated region, nitrate was undetectable between surface and 160–180 m, while regenerated nitrogen (nitrite and ammonium) only revealed some traces (<20 nmoles l−1), even in the subsurface maximum. Integrated nitrate over the photic layer, which reached 165 m, was close to zero. In spite of this severe nitrogen-depletion, phosphate was always present at significant concentrations (≈0.1 μmoles l−1), while silicate maintained at low but classical oceanic levels (≈1 μmoles l−1). In contrast, the Marquesas region (MAR) at west and Chilean upwelling (UPW) at east were characterized by large nutrient contents one hundred to one thousand fold higher than in the SPG. Distribution of surface chlorophyll concentration reflected this gradient of nitrate availability. The lowest value (0.023 nmoles l−1) was measured in the centre of the SPG, where integrated chlorophyll over the photic layer was very weak (≈10 mg m−2), since a great part (up to 50%) of the deep chlorophyll maximum (DCM) was located below the 1% light. But, because of the relative high concentration encountered in the DCM (0.2 μg l−1), chlorophyll a content over the photic layer varied much less (by a factor 2 to 5) than the nitrate content. In contrast to chlorophyll a, integrated content of particulate organic matter (POM) remained more or less constant along the investigated area (500 mmoles m−2, 60 mmoles m−2 and 3.5 mmoles m−2 for particulate organic carbon, particulate organic nitrogen and particulate organic phosphorus, respectively), except in the upwelling where values were two fold higher. Extensive comparison has shown that glass fiber GF/F filters efficiency collected particulate chlorophyll, while a significant fraction of POM (up to 50%) passed trough this filter and was retained by 0.2 μm Teflon membrane. The most striking feature was the large accumulation of dissolved organic matter (DOM) in the SPG relative to surrounding waters, especially dissolved organic carbon (DOC) where concentrations were at levels rarely measured in oceanic waters (>100 μmoles l−1). Due to this large pool of DOM over the whole photic layer of the SPG, integrated values followed an opposite geographical pattern than this of inorganic nutrients with a large accumulation within the centre of the SPG. While suspended particulate matter in the mixed layer had C/N ratio largely conform to Redfield stoichiometry (C/N≈6.6), marked deviations were observed in this excess DOM (C/N≈16 to 23). The existence of C-rich dissolved organic matter is recognized as a feature typical of oligotrophic waters, requiring the over consumption of carbon. Thus, in spite of strong nitrate-depletion leading to low chlorophyll biomass, the closed ecosystem of the SPG can produce a large amount of carbon. The implications of this finding are discussed, the conclusion being that, due to the lack of seasonal vertical mixing and weak lateral advection, the dissolved organic carbon biologically produced can be accumulated and stored in the photic layer for a very long period.


2005 ◽  
Vol 62 (2) ◽  
pp. 472-481 ◽  
Author(s):  
Jennifer L Klug

In aquatic systems, the presence of colored dissolved organic matter (DOM) may affect algal growth in numerous ways. This paper focuses on the effects of DOM on resource availability. DOM contains nitrogen and phosphorus, which may become available following microbial or photochemical degradation. Also, addition of DOM may stimulate bacterial growth, which in turn may change the availability of nitrogen, phosphorus, and inorganic carbon to algae. Experiments conducted in a moderately colored lake showed that the effect of DOM on algal growth depended on the amount of nutrients present in the peat extract and on bacterial response to DOM. There was evidence for competition for phosphorus between algae and bacteria in some treatments. In addition, when both bacteria growth and algal growth were high, bacterial respiration of DOM alleviated algal carbon limitation by providing algae with an inorganic carbon source. Thus, the degree to which bacteria are stimulated by the addition of DOM will affect the amount of phosphorus and inorganic carbon available for algal growth. These results suggest that part of the difficulty in predicting algal response to changes in DOM and nutrient concentration may be due partially to variability in bacterial responses.


2018 ◽  
Vol 15 (13) ◽  
pp. 4215-4232 ◽  
Author(s):  
Sophie Bonnet ◽  
Mathieu Caffin ◽  
Hugo Berthelot ◽  
Olivier Grosso ◽  
Mar Benavides ◽  
...  

Abstract. Here we report N2 fixation rates from a ∼ 4000 km transect in the western and central tropical South Pacific, a particularly undersampled region in the world ocean. Water samples were collected in the euphotic layer along a west to east transect from 160∘ E to 160∘ W that covered contrasting trophic regimes, from oligotrophy in the Melanesian archipelago (MA) waters to ultra-oligotrophy in the South Pacific Gyre (GY) waters. N2 fixation was detected at all 17 sampled stations with an average depth-integrated rate of 631 ± 286 µmolNm-2d-1 (range 196–1153 µmolNm-2d-1) in MA waters and of 85 ± 79 µmolNm-2d-1 (range 18–172 µmolNm-2d-1) in GY waters. Two cyanobacteria, the larger colonial filamentous Trichodesmium and the smaller UCYN-B, dominated the enumerated diazotroph community (> 80 %) and gene expression of the nifH gene (cDNA > 105 nifH copies L−1) in MA waters. Single-cell isotopic analyses performed by nanoscale secondary ion mass spectrometry (nanoSIMS) at selected stations revealed that Trichodesmium was always the major contributor to N2 fixation in MA waters, accounting for 47.1–83.8 % of bulk N2 fixation. The most plausible environmental factors explaining such exceptionally high rates of N2 fixation in MA waters are discussed in detail, emphasizing the role of macro- and micro-nutrient (e.g., iron) availability, seawater temperature and currents.


2019 ◽  
Vol 16 (9) ◽  
pp. 2033-2047 ◽  
Author(s):  
Alexandra N. Loginova ◽  
Sören Thomsen ◽  
Marcus Dengler ◽  
Jan Lüdke ◽  
Anja Engel

Abstract. The eastern tropical South Pacific (ETSP) hosts the Peruvian upwelling system, which represents one of the most productive areas in the world ocean. High primary production followed by rapid heterotrophic utilization of organic matter supports the formation of one of the most intense oxygen minimum zones (OMZs) in the world ocean, where dissolved oxygen (O2) concentrations reach less than 1 µmol kg−1. The high productivity leads to an accumulation of dissolved organic matter (DOM) in the surface layers that may serve as a substrate for heterotrophic respiration. However, the importance of DOM utilization for O2 respiration in the Peruvian upwelling system in general and for shaping the upper oxycline in particular remains unclear so far. This study reports the first estimates of diapycnal fluxes and supply of O2, dissolved organic carbon (DOC), dissolved organic nitrogen, dissolved hydrolysable amino acids (DHAA) and dissolved combined carbohydrates (DCCHO) for the ETSP off Peru. Diapycnal flux and supply estimates were obtained by combining measured vertical diffusivities and solute concentration gradients. They were analysed together with the molecular composition of DCCHO and DHAA to infer the transport of labile DOM into the upper OMZ and the potential role of DOM utilization for the attenuation of the diapycnal O2 flux that ventilates the OMZ. The observed diapycnal O2 flux (50 mmol O2 m−2 d−1 at maximum) was limited to the upper 80 m of the water column; the O2 supply of ∼1 µmol kg−1 d−1 was comparable to previously published O2 consumption rates for the North and South Pacific OMZs. The diapycnal DOM flux (31 mmol C m−2 d−1 at maximum) was limited to ∼30 m water depth, suggesting that the labile DOM is extensively consumed within the upper part of the shallow oxycline off Peru. The analyses of DCCHO and DHAA composition support this finding, suggesting that DOM undergoes comprehensive remineralization within the upper part of the oxycline, as the DOM within the core of the OMZ was found to be largely altered. Estimated by a simple equation for carbon combustion, aerobic respiration of DCCHO and DHAA, supplied by diapycnal mixing (0.46 µmol kg−1 d−1 at maximum), could account for up to 38 % of the diapycnal O2 supply in the upper oxycline, which suggests that DOM utilization plays a significant role for shaping the upper oxycline in the ETSP.


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