Dataset Information

Climate change promotes parasitism in a coral symbiosis.

ABSTRACT: Coastal oceans are increasingly eutrophic, warm and acidic through the addition of anthropogenic nitrogen and carbon, respectively. Among the most sensitive taxa to these changes are scleractinian corals, which engineer the most biodiverse ecosystems on Earth. Corals' sensitivity is a consequence of their evolutionary investment in symbiosis with the dinoflagellate alga, Symbiodinium. Together, the coral holobiont has dominated oligotrophic tropical marine habitats. However, warming destabilizes this association and reduces coral fitness. It has been theorized that, when reefs become warm and eutrophic, mutualistic Symbiodinium sequester more resources for their own growth, thus parasitizing their hosts of nutrition. Here, we tested the hypothesis that sub-bleaching temperature and excess nitrogen promotes symbiont parasitism by measuring respiration (costs) and the assimilation and translocation of both carbon (energy) and nitrogen (growth; both benefits) within Orbicella faveolata hosting one of two Symbiodinium phylotypes using a dual stable isotope tracer incubation at ambient (26?°C) and sub-bleaching (31?°C) temperatures under elevated nitrate. Warming to 31?°C reduced holobiont net primary productivity (NPP) by 60% due to increased respiration which decreased host %carbon by 15% with no apparent cost to the symbiont. Concurrently, Symbiodinium carbon and nitrogen assimilation increased by 14 and 32%, respectively while increasing their mitotic index by 15%, whereas hosts did not gain a proportional increase in translocated photosynthates. We conclude that the disparity in benefits and costs to both partners is evidence of symbiont parasitism in the coral symbiosis and has major implications for the resilience of coral reefs under threat of global change.

SUBMITTER: Baker DM

PROVIDER: S-EPMC5864192 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Climate change promotes parasitism in a coral symbiosis.

Baker David M DM Freeman Christopher J CJ Wong Jane C Y JCY Fogel Marilyn L ML Knowlton Nancy N

The ISME journal 20180129 3

Coastal oceans are increasingly eutrophic, warm and acidic through the addition of anthropogenic nitrogen and carbon, respectively. Among the most sensitive taxa to these changes are scleractinian corals, which engineer the most biodiverse ecosystems on Earth. Corals' sensitivity is a consequence of their evolutionary investment in symbiosis with the dinoflagellate alga, Symbiodinium. Together, the coral holobiont has dominated oligotrophic tropical marine habitats. However, warming destabilizes ...[more]

PMID: 29379177

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Project description:Global warming impacts diverse organisms not only directly but also indirectly via other organisms with which they interact. Recently, the possibility that elevated temperatures resulting from global warming may substantially affect biodiversity through disrupting mutualistic/parasitic associations has been highlighted. Here we report an experimental demonstration that global warming can affect a pest insect via suppression of its obligate bacterial symbiont. The southern green stinkbug Nezara viridula depends on a specific gut bacterium for its normal growth and survival. When the insects were reared inside or outside a simulated warming incubator wherein temperature was controlled at 2.5°C higher than outside, the insects reared in the incubator exhibited severe fitness defects (i.e., retarded growth, reduced size, yellowish body color, etc.) and significant reduction of symbiont population, particularly in the midsummer season, whereas the insects reared outside did not. Rearing at 30°C or 32.5°C resulted in similar defective phenotypes of the insects, whereas no adult insects emerged at 35°C. Notably, experimental symbiont suppression by an antibiotic treatment also induced similar defective phenotypes of the insects, indicating that the host's defective phenotypes are attributable not to the heat stress itself but to the suppression of the symbiont population induced by elevated temperature. These results strongly suggest that high temperature in the midsummer season negatively affects the insects not directly but indirectly via the heat-vulnerable obligate bacterial symbiont, which highlights the practical relevance of mutualism collapse in this warming world. Climate change is among the biggest environmental issues in the contemporary world, and its impact on the biodiversity and ecosystem is not only of scientific interest but also of practical concern for the general public. On the basis of our laboratory data obtained under strictly controlled environmental conditions and our simulated warming data obtained in seminatural settings (elevated 2.5°C above the normal temperature), we demonstrate here that Nezara viridula, the notorious stinkbug pest, suffers serious fitness defects in the summer season under the simulated warming conditions, wherein high temperature acts on the insect not directly but indirectly via suppression of its obligate gut bacterium. Our finding highlights that heat-susceptible symbionts can be the "Achilles' heel" of symbiont-dependent organisms under climate change conditions.

Dataset Information

Climate change promotes parasitism in a coral symbiosis.

Publications

Climate change promotes parasitism in a coral symbiosis.

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