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Chemosymbiotic bivalves contribute to the nitrogen budget of seagrass ecosystems.

ABSTRACT: In many seagrass sediments, lucinid bivalves and their sulfur-oxidizing symbionts are thought to underpin key ecosystem functions, but little is known about their role in nutrient cycles, particularly nitrogen. We used natural stable isotopes, elemental analyses, and stable isotope probing to study the ecological stoichiometry of a lucinid symbiosis in spring and fall. Chemoautotrophy appeared to dominate in fall, when chemoautotrophic carbon fixation rates were up to one order of magnitude higher as compared with the spring, suggesting a flexible nutritional mutualism. In fall, an isotope pool dilution experiment revealed carbon limitation of the symbiosis and ammonium excretion rates up to tenfold higher compared with fluxes reported for nonsymbiotic marine bivalves. These results provide evidence that lucinid bivalves can contribute substantial amounts of ammonium to the ecosystem. Given the preference of seagrasses for this nitrogen source, lucinid bivalves' contribution may boost productivity of these important blue carbon ecosystems.

SUBMITTER: Cardini U

PROVIDER: S-EPMC6863832 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Chemosymbiotic bivalves contribute to the nitrogen budget of seagrass ecosystems.

Cardini Ulisse U Bartoli Marco M Lücker Sebastian S Mooshammer Maria M Polzin Julia J Lee Raymond W RW Micić Vesna V Hofmann Thilo T Weber Miriam M Petersen Jillian M JM

The ISME journal 20190808 12

In many seagrass sediments, lucinid bivalves and their sulfur-oxidizing symbionts are thought to underpin key ecosystem functions, but little is known about their role in nutrient cycles, particularly nitrogen. We used natural stable isotopes, elemental analyses, and stable isotope probing to study the ecological stoichiometry of a lucinid symbiosis in spring and fall. Chemoautotrophy appeared to dominate in fall, when chemoautotrophic carbon fixation rates were up to one order of magnitude high ...[more]

PMID: 31395953

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Project description:In seagrass sediments, lucinid bivalves and their chemoautotrophic bacterial symbionts consume H2S, relying indirectly on the plant productivity for the presence of the reduced chemical. Additionally, the role of lucinid bivalves in N provisioning to the plant (through N2 fixation by the symbionts) was hypothesized. Thus, lucinids may contribute to sediment detoxification and plant fitness. Seagrasses are subject to ever-increasing human pressure in coastal environments. Here, disentangling nested interactions between chemosynthetic lucinid bivalves and seagrass exposed to pollution may help to understand seagrass ecosystem dynamics and to develop successful seagrass restoration programs that consider the roles of animal-microbe symbioses. We evaluated the capacity of lucinid bivalves (Loripes orbiculatus) to promote nutrient cycling and seagrass (Cymodocea nodosa) growth during a 6-week mesocosm experiment. A fully crossed design was used to test for the effect of sediment contamination (metals, nutrients, and hydrocarbons) on plant and bivalve (alone or interacting) fitness, assessed by mortality, growth, and photosynthetic efficiency, and for the effect of their nested interaction on sediment biogeochemistry. Plants performed better in the contaminated sediment, where a larger pool of dissolved nitrogen combined with the presence of other trace elements allowed for an improved photosynthetic efficiency. In fact, pore water nitrogen accumulated during the experiment in the controls, while it was consumed in the contaminated sediment. This trend was accentuated when lucinids were present. Concurrently, the interaction between clams and plants benefitted both organisms and promoted plant growth irrespective of the sediment type. In particular, the interaction with lucinid clams resulted in higher aboveground biomass of C. nodosa in terms of leaf growth, leaf surface, and leaf biomass. Our results consolidate the notion that nested interactions involving animal-microbe associations promote ecosystem functioning, and potentially help designing unconventional seagrass restoration strategies that exploit chemosynthetic symbioses.

Project description:The N cycle of arid ecosystems is influenced by low soil organic matter, high soil pH, and extremes in water potential and temperature that lead to open canopies and development of biological soil crusts (biocrusts). We investigated the effects of N amendment on soil microbial dynamics in a Larrea tridentata-Ambrosia dumosa shrubland site in southern Nevada USA. Sites were fertilized with a NO3-NH4 mix at 0, 7, and 15 kg N ha(-1) y(-1) from March 2012 to March 2013. In March 2013, biocrust (0-0.5 cm) and bulk soils (0-10 cm) were collected beneath Ambrosia canopies and in the interspaces between plants. Biomass responses were assessed as bacterial and fungal SSU rRNA gene copy number and chlorophyll a concentration. Metabolic responses were measured by five ecoenzyme activities and rates of N transformation. By most measures, nutrient availability, microbial biomass, and process rates were greater in soils beneath the shrub canopy compared to the interspace between plants, and greater in the surface biocrust horizon compared to the deeper 10 cm soil profile. Most measures responded positively to experimental N addition. Effect sizes were generally greater for bulk soil than biocrust. Results were incorporated into a meta-analysis of arid ecosystem responses to N amendment that included data from 14 other studies. Effect sizes were calculated for biomass and metabolic responses. Regressions of effect sizes, calculated for biomass, and metabolic responses, showed similar trends in relation to N application rate and N load (rate × duration). The critical points separating positive from negative treatment effects were 88 kg ha(-1) y(-1) and 159 kg ha(-1), respectively, for biomass, and 70 kg ha(-1) y(-1) and 114 kg ha(-1), respectively, for metabolism. These critical values are comparable to those for microbial biomass, decomposition rates and respiration reported in broader meta-analyses of N amendment effects in mesic ecosystems. However, large effect sizes at low N addition rates indicate that arid ecosystems are sensitive to modest increments in anthropogenic N deposition.

Dataset Information

Chemosymbiotic bivalves contribute to the nitrogen budget of seagrass ecosystems.

Publications

Chemosymbiotic bivalves contribute to the nitrogen budget of seagrass ecosystems.

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