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      Natural volcanic CO 2 seeps reveal future trajectories for host–microbial associations in corals and sponges

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          Abstract

          Atmospheric carbon dioxide (CO 2) levels are rapidly rising causing an increase in the partial pressure of CO 2 ( pCO 2) in the ocean and a reduction in pH known as ocean acidification (OA). Natural volcanic seeps in Papua New Guinea expel 99% pure CO 2 and thereby offer a unique opportunity to explore the effects of OA in situ. The corals Acropora millepora and Porites cylindrica were less abundant and hosted significantly different microbial communities at the CO 2 seep than at nearby control sites <500 m away. A primary driver of microbial differences in A. millepora was a 50% reduction of symbiotic Endozoicomonas. This loss of symbiotic taxa from corals at the CO 2 seep highlights a potential hurdle for corals to overcome if they are to adapt to and survive OA. In contrast, the two sponges Coelocarteria singaporensis and Cinachyra sp. were ∼40-fold more abundant at the seep and hosted a significantly higher relative abundance of Synechococcus than sponges at control sites. The increase in photosynthetic microbes at the seep potentially provides these species with a nutritional benefit and enhanced scope for growth under future climate scenarios (thus, flexibility in symbiosis may lead to a larger niche breadth). The microbial community in the apparently pCO 2-sensitive sponge species S. massa was not significantly different between sites. These data show that responses to elevated pCO 2 are species-specific and that the stability and flexibility of microbial partnerships may have an important role in shaping and contributing to the fitness and success of some hosts.

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          Most cited references27

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          Volcanic carbon dioxide vents show ecosystem effects of ocean acidification.

          The atmospheric partial pressure of carbon dioxide (p(CO(2))) will almost certainly be double that of pre-industrial levels by 2100 and will be considerably higher than at any time during the past few million years. The oceans are a principal sink for anthropogenic CO(2) where it is estimated to have caused a 30% increase in the concentration of H(+) in ocean surface waters since the early 1900s and may lead to a drop in seawater pH of up to 0.5 units by 2100 (refs 2, 3). Our understanding of how increased ocean acidity may affect marine ecosystems is at present very limited as almost all studies have been in vitro, short-term, rapid perturbation experiments on isolated elements of the ecosystem. Here we show the effects of acidification on benthic ecosystems at shallow coastal sites where volcanic CO(2) vents lower the pH of the water column. Along gradients of normal pH (8.1-8.2) to lowered pH (mean 7.8-7.9, minimum 7.4-7.5), typical rocky shore communities with abundant calcareous organisms shifted to communities lacking scleractinian corals with significant reductions in sea urchin and coralline algal abundance. To our knowledge, this is the first ecosystem-scale validation of predictions that these important groups of organisms are susceptible to elevated amounts of p(CO(2)). Sea-grass production was highest in an area at mean pH 7.6 (1,827 (mu)atm p(CO(2))) where coralline algal biomass was significantly reduced and gastropod shells were dissolving due to periods of carbonate sub-saturation. The species populating the vent sites comprise a suite of organisms that are resilient to naturally high concentrations of p(CO(2)) and indicate that ocean acidification may benefit highly invasive non-native algal species. Our results provide the first in situ insights into how shallow water marine communities might change when susceptible organisms are removed owing to ocean acidification.
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            Ocean acidification causes bleaching and productivity loss in coral reef builders.

            Ocean acidification represents a key threat to coral reefs by reducing the calcification rate of framework builders. In addition, acidification is likely to affect the relationship between corals and their symbiotic dinoflagellates and the productivity of this association. However, little is known about how acidification impacts on the physiology of reef builders and how acidification interacts with warming. Here, we report on an 8-week study that compared bleaching, productivity, and calcification responses of crustose coralline algae (CCA) and branching (Acropora) and massive (Porites) coral species in response to acidification and warming. Using a 30-tank experimental system, we manipulated CO(2) levels to simulate doubling and three- to fourfold increases [Intergovernmental Panel on Climate Change (IPCC) projection categories IV and VI] relative to present-day levels under cool and warm scenarios. Results indicated that high CO(2) is a bleaching agent for corals and CCA under high irradiance, acting synergistically with warming to lower thermal bleaching thresholds. We propose that CO(2) induces bleaching via its impact on photoprotective mechanisms of the photosystems. Overall, acidification impacted more strongly on bleaching and productivity than on calcification. Interestingly, the intermediate, warm CO(2) scenario led to a 30% increase in productivity in Acropora, whereas high CO(2) lead to zero productivity in both corals. CCA were most sensitive to acidification, with high CO(2) leading to negative productivity and high rates of net dissolution. Our findings suggest that sensitive reef-building species such as CCA may be pushed beyond their thresholds for growth and survival within the next few decades whereas corals will show delayed and mixed responses.
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              Stress tolerance in plants via habitat-adapted symbiosis.

              We demonstrate that native grass species from coastal and geothermal habitats require symbiotic fungal endophytes for salt and heat tolerance, respectively. Symbiotically conferred stress tolerance is a habitat-specific phenomenon with geothermal endophytes conferring heat but not salt tolerance, and coastal endophytes conferring salt but not heat tolerance. The same fungal species isolated from plants in habitats devoid of salt or heat stress did not confer these stress tolerances. Moreover, fungal endophytes from agricultural crops conferred disease resistance and not salt or heat tolerance. We define habitat-specific, symbiotically-conferred stress tolerance as habitat-adapted symbiosis and hypothesize that it is responsible for the establishment of plants in high-stress habitats. The agricultural, coastal and geothermal plant endophytes also colonized tomato (a model eudicot) and conferred disease, salt and heat tolerance, respectively. In addition, the coastal plant endophyte colonized rice (a model monocot) and conferred salt tolerance. These endophytes have a broad host range encompassing both monocots and eudicots. Interestingly, the endophytes also conferred drought tolerance to plants regardless of the habitat of origin. Abiotic stress tolerance correlated either with a decrease in water consumption or reactive oxygen sensitivity/generation but not to increased osmolyte production. The ability of fungal endophytes to confer stress tolerance to plants may provide a novel strategy for mitigating the impacts of global climate change on agricultural and native plant communities.
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                Author and article information

                Journal
                ISME J
                ISME J
                The ISME Journal
                Nature Publishing Group
                1751-7362
                1751-7370
                April 2015
                17 October 2014
                1 April 2015
                : 9
                : 4
                : 894-908
                Affiliations
                [1 ]Australian Institute of Marine Science, P.M.B. 3 , Townville, Queensland, Australia
                Author notes
                [* ]A healthy and Resilient GBR, Australian Institute of Marine Science, PMB 3 Townsville Mail Centre , Townsville, Queensland 4810, Australia. E-mail: n.webster@ 123456aims.gov.au
                Article
                ismej2014188
                10.1038/ismej.2014.188
                4817704
                25325380
                c292a4b4-dce1-4b90-a045-9135d228480c
                Copyright © 2015 International Society for Microbial Ecology

                This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/

                History
                : 22 May 2014
                : 18 August 2014
                : 21 August 2014
                Categories
                Original Article

                Microbiology & Virology
                Microbiology & Virology

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