| 1. |
- Cardini, Ulisse, et al.
(författare)
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Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions
- 2015
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Ingår i: Proceedings of the Royal Society of London. Biological Sciences. - : The Royal Society. - 0962-8452 .- 1471-2954. ; 282:1818
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Tidskriftsartikel (refereegranskat)abstract
- Functional traits define species by their ecological role in the ecosystem. Animals themselves are host-microbe ecosystems (holobionts), and the application of ecophysiological approaches can help to understand their functioning. In hard coral holobionts, communities of dinitrogen (N-2)-fixing prokaryotes (diazotrophs) may contribute a functional trait by providing bioavailable nitrogen (N) that could sustain coral productivity under oligotrophic conditions. This study quantified N-2 fixation by diazotrophs associated with four genera of hermatypic corals on a northern Red Sea fringing reef exposed to high seasonality. We found N-2 fixation activity to be 5- to 10-fold higher in summer, when inorganic nutrient concentrations were lowest and water temperature and light availability highest. Concurrently, coral gross primary productivity remained stable despite lower Symbiodinium densities and tissue chlorophyll a contents. In contrast, chlorophyll a content per Symbiodinium cell increased from spring to summer, suggesting that algal cells overcame limitation of N, an essential element for chlorophyll synthesis. In fact, N-2 fixation was positively correlated with coral productivity in summer, when its contribution was estimated to meet 11% of the Symbiodinium N requirements. These results provide evidence of an important functional role of diazotrophs in sustaining coral productivity when alternative external N sources are scarce.
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| 2. |
- Cardini, Ulisse, et al.
(författare)
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Microbial dinitrogen fixation in coral holobionts exposed to thermal stress and bleaching
- 2016
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Ingår i: Environmental Microbiology. - : Wiley. - 1462-2912 .- 1462-2920. ; 18:8, s. 2620-2633
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Tidskriftsartikel (refereegranskat)abstract
- Coral holobionts (i.e., coral-algal-prokaryote symbioses) exhibit dissimilar thermal sensitivities that may determine which coral species will adapt to global warming. Nonetheless, studies simultaneously investigating the effects of warming on all holobiont members are lacking. Here we show that exposure to increased temperature affects key physiological traits of all members (herein: animal host, zooxanthellae and diazotrophs) of both Stylophora pistillata and Acropora hemprichii during and after thermal stress. S. pistillata experienced severe loss of zooxanthellae (i.e., bleaching) with no net photosynthesis at the end of the experiment. Conversely, A. hemprichii was more resilient to thermal stress. Exposure to increased temperature (+ 6 degrees C) resulted in a drastic increase in daylight dinitrogen (N-2) fixation, particularly in A. hemprichii (threefold compared with controls). After the temperature was reduced again to in situ levels, diazotrophs exhibited a reversed diel pattern of activity, with increased N-2 fixation rates recorded only in the dark, particularly in bleached S. pistillata (twofold compared to controls). Concurrently, both animal hosts, but particularly bleached S. pistillata, reduced both organic matter release and heterotrophic feeding on picoplankton. Our findings indicate that physiological plasticity by coral-associated diazotrophs may play an important role in determining the response of coral holobionts to ocean warming.
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| 3. |
- Dittami, Simon M., et al.
(författare)
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A community perspective on the concept of marine holobionts : current status, challenges, and future directions
- 2021
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Ingår i: PeerJ. - : PEERJ INC. - 2167-8359. ; 9
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Tidskriftsartikel (refereegranskat)abstract
- Host-microbe interactions play crucial roles in marine ecosystems. However, we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help to describe and understand these complex systems. It posits that a host and its associated microbiota with which it interacts, form a holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences. Given the connectivity and the unexplored biodiversity specific to marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances, e.g., the development of controlled experimental model systems for holobionts from all major lineages and the modeling of (info)chemical-mediated interactions between organisms. Here we propose that one significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This first step is crucial to decipher the main drivers of the dynamics and evolution of holobionts and to account for the holobiont concept in applied areas, such as the conservation, management, and exploitation of marine ecosystems and resources, where practical solutions to predict and mitigate the impact of human activities are more important than ever.
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| 4. |
- Marzocchi, Ugo, et al.
(författare)
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Zebra Mussel Holobionts Fix and Recycle Nitrogen in Lagoon Sediments
- 2021
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Ingår i: Frontiers in Microbiology. - : Frontiers Media SA. - 1664-302X. ; 11
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Tidskriftsartikel (refereegranskat)abstract
- Bivalves are ubiquitous filter-feeders able to alter ecosystems functions. Their impact on nitrogen (N) cycling is commonly related to their filter-feeding activity, biodeposition, and excretion. A so far understudied impact is linked to the metabolism of the associated microbiome that together with the host constitute the mussel's holobiont. Here we investigated how colonies of the invasive zebra mussel (Dreissena polymorpha) alter benthic N cycling in the shallow water sediment of the largest European lagoon (the Curonian Lagoon). A set of incubations was conducted to quantify the holobiont's impact and to quantitatively compare it with the indirect influence of the mussel on sedimentary N transformations. Zebra mussels primarily enhanced the recycling of N to the water column by releasing mineralized algal biomass in the form of ammonium and by stimulating dissimilatory nitrate reduction to ammonium (DNRA). Notably, however, not only denitrification and DNRA, but also dinitrogen (N-2) fixation was measured in association with the holobiont. The diazotrophic community of the holobiont diverged substantially from that of the water column, suggesting a unique niche for N-2 fixation associated with the mussels. At the densities reported in the lagoon, mussel-associated N-2 fixation may account for a substantial (and so far, overlooked) source of bioavailable N. Our findings contribute to improve our understanding on the ecosystem-level impact of zebra mussel, and potentially, of its ability to adapt to and colonize oligotrophic environments.
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| 5. |
- Politi, Tobia, et al.
(författare)
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A bioturbator, a holobiont, and a vector: The multifaceted role of Chironomus plumosus in shaping N-cycling
- 2021
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Ingår i: Freshwater Biology. - : Wiley. - 0046-5070 .- 1365-2427. ; 66:6, s. 1036-1048
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Tidskriftsartikel (refereegranskat)abstract
- Tube-dwelling chironomid larvae are among the few taxa that can withstand and thrive in the organic-rich sediments typical of eutrophic freshwater ecosystems. They can have multiple effects on microbial nitrogen (N) cycling in burrow environments, but such effects cease when chironomid larvae undergo metamorphosis into flying adults and leave the sediment. Here we investigated the ecological role of Chironomus plumosus by exploring the effect of its different life stages (as larva and adult midge) on microbial N transformations in a shallow freshwater lagoon by means of combined biogeochemical and molecular approaches. Results suggest that sediment bioturbation by chironomid larvae produce contrasting effects on nitrate ((Formula presented.))-reduction processes. Denitrification was the dominant pathway of (Formula presented.) reduction (>90%), primarily fuelled by (Formula presented.) from bottom water. In addition to pumping (Formula presented.) -rich bottom water within the burrows, chironomid larvae host microbiota capable of (Formula presented.) reduction. However, the contribution of larval microbiota is lower than that of microbes inhabiting the burrow walls. Interestingly, dinitrogen fixation co-occurred with (Formula presented.) reduction processes, indicating versatility of the larvae's microbial community. Assuming all larvae (averaging 1,800 ind./m ) leave the sediment following metamorphosis into flying adults, we estimated a displacement of 47,787µmol of organic N/m from the sediment to the atmosphere during adult emergence. This amount of particulate organic N is similar to the entire N removal stimulated by larvae denitrification over a period of 20days. Finally, the detection of N-cycling marker genes in flying adults suggests that these insects retain N-cycling microbes during metamorphosis and migration to the aerial and terrestrial ecosystems. This study provides evidence that chironomids have a multifaceted role in shaping the N cycle of aquatic ecosystems. 2 2
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| 6. |
- Politi, Tobia, 1988, et al.
(författare)
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Direct contribution of invertebrate holobionts to methane release from coastal sediments
- 2023
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Ingår i: Limnology And Oceanography Letters. - 2378-2242. ; 8:6, s. 876-84
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Tidskriftsartikel (refereegranskat)abstract
- Sediment macrofauna play a vital role in sustaining aquatic food webs and biogeochemical cycles. Previous research demonstrated that bioturbation indirectly affects methane (CH4) dynamics through mobilization of porewater and alteration of microbial processes in the surrounding sediment. However, little is known on the direct contribution of macrofauna holobionts (the assemblage of invertebrate host and associated microbiome) to biogeochemical fluxes. Here, we investigated how 19 taxa of macrofauna holobionts, from different estuarine habitats spanning 40° to 63° latitude, directly contribute to CH4 fluxes. Deep burrowing infauna and deposit feeders were responsible for the highest CH4 production, whereas epifauna and filter feeders promoted oxidative CH4 consumption. Among the different environmental parameters, salinity was inversely correlated with CH4 production by macrofauna holobionts, with the process suppressed at high salinity (≥ 33). This study provides empirical evidence on how functional traits and environmental factors influence sediment invertebrates' contribution to CH4 fluxes.
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| 7. |
- Samuiloviene, Aurelija, et al.
(författare)
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The Effect of Chironomid Larvae on Nitrogen Cycling and Microbial Communities in Soft Sediments
- 2019
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Ingår i: Water. - : MDPI AG. - 2073-4441. ; 11:9
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Tidskriftsartikel (refereegranskat)abstract
- The combination of biogeochemical methods and molecular techniques has the potential to uncover the black-box of the nitrogen (N) cycle in bioturbated sediments. Advanced biogeochemical methods allow the quantification of the process rates of different microbial processes, whereas molecular tools allow the analysis of microbial diversity (16S rRNA metabarcoding) and activity (marker genes and transcripts) in biogeochemical hot-spots such as the burrow wall or macrofauna guts. By combining biogeochemical and molecular techniques, we analyzed the role of tube-dwelling Chironomus plumosus (Insecta, Diptera) larvae on nitrification and nitrate reduction processes in a laboratory experiment with reconstructed sediments. We hypothesized that chironomid larvae stimulate these processes and host bacteria actively involved in N-cycling. Our results suggest that chironomid larvae significantly enhance the recycling of ammonium (80.5 +/- 48.7 mu mol m(-2) h(-1)) and the production of dinitrogen (420.2 +/- 21.4 mu mol m(-2) h(-1)) via coupled nitrification-denitrification and the consumption of water column nitrates. Besides creating oxygen microniches in ammonium-rich subsurface sediments via burrow digging and ventilation, chironomid larvae serve as hot-spots of microbial communities involved in N-cycling. The quantification of functional genes showed a significantly higher potential for microbial denitrification and nitrate ammonification in larvae as compared to surrounding sediments. Future studies may further scrutinize N transformation rates associated with intimate macrofaunal-bacteria associations.
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| 8. |
- Zilius,, Mindaugas, et al.
(författare)
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N2 fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont
- 2020
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Ingår i: Scientific Reports. - : Springer Science and Business Media LLC. - 2045-2322. ; 10:1
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Tidskriftsartikel (refereegranskat)abstract
- Mangrove forests are among the most productive and diverse ecosystems on the planet, despite limited nitrogen (N) availability. Under such conditions, animal-microbe associations (holobionts) are often key to ecosystem functioning. Here, we investigated the role of fiddler crabs and their carapace-associated microbial biofilm as hotspots of microbial N transformations and sources of N within the mangrove ecosystem. 16S rRNA gene and metagenomic sequencing provided evidence of a microbial biofilm dominated by Cyanobacteria, Alphaproteobacteria, Actinobacteria, and Bacteroidota with a community encoding both aerobic and anaerobic pathways of the N cycle. Dinitrogen (N2) fixation was among the most commonly predicted process. Net N fluxes between the biofilm-covered crabs and the water and microbial N transformation rates in suspended biofilm slurries portray these holobionts as a net N2 sink, with N2 fixation exceeding N losses, and as a significant source of ammonium and dissolved organic N to the surrounding environment. N stable isotope natural abundances of fiddler crab carapace-associated biofilms were within the range expected for fixed N, further suggesting active microbial N2 fixation. These results extend our knowledge on the diversity of invertebrate-microbe associations, and provide a clear example of how animal microbiota can mediate a plethora of essential biogeochemical processes in mangrove ecosystems.
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| 9. |
- Zilius, Mindaugas, et al.
(författare)
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Partitioning benthic nitrogen cycle processes among three common macrofauna holobionts
- 2022
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Ingår i: Biogeochemistry. - : Springer Science and Business Media LLC. - 0168-2563 .- 1573-515X. ; 157:2, s. 193-213
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Tidskriftsartikel (refereegranskat)abstract
- The effects of single macrofauna taxa on benthic nitrogen (N) cycling have been extensively studied, whereas how macrofaunal communities affect N-related processes remains poorly explored. In this study, we characterized benthic N-cycling in bioturbated sediments of the oligotrophic Öre Estuary (northern Baltic Sea). Solute fluxes and N transformations (N2 fixation, denitrification and dissimilative nitrate reduction to ammonium [DNRA]) were measured in sediments and macrofauna-associated microbes (holobionts) to partition the role of three dominant taxa (the filter feeder Limecola balthica, the deep deposit feeder Marenzelleria spp., and the surface deposit feeder Monoporeia affinis) in shaping N-cycling. In the studied area, benthic macrofauna comprised a low diversity community with dominance of the three taxa, which are widespread and dominant in the Baltic. The biomass of these taxa in macrofaunal community explained up to 30% of variation in measured biogeochemical processes, confirming their important role in ecosystem functioning. The results also show that these taxa significantly contributed to the benthic metabolism and N-cycling (direct effect) as well as to sediments bioturbation with positive feedback to dissimilative nitrate reduction (indirect effect). Taken together, these functions promoted a reuse of nutrients at the benthic level, limiting net losses (e.g. denitrification) and effluxes to bottom water. Finally, the detection of multiple N transformations in macrofauna holobionts suggested a community-associated versatile microbiome, however, its role was of minor importance as compared to the activity of sediment-associated microbial communities. The present study highlights hidden and interactive effects among microbes and macrofauna, which should be considered analysing benthic functioning.
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