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Climate Change Affects Key Nitrogen-Fixing Bacterial Populations on Coral Reefs

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Climate Change Affects Key Nitrogen-Fixing Bacterial Populations on Coral Reefs The ISME Journal (2014) 8, 2272–2279 & 2014 International Society for Microbial Ecology All rights reserved 1751-7362/14 www.nature.com/ismej ORIGINAL ARTICLE Climate change affects key nitrogen-fixing bacterial populations on coral reefs Henrique F Santos1,2, Fla´via L Carmo1, Gustavo Duarte3, Francisco Dini-Andreote2, Clovis B Castro3,4, Alexandre S Rosado1,4, Jan Dirk van Elsas2 and Raquel S Peixoto1,4 1LEMM, Laboratory of Molecular Microbial Ecology, Institute of Microbiology Paulo de Go´es, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil; 2Department of Microbial Ecology, Centre for Ecological and Evolutionary Studies, University of Groningen, Groningen, The Netherlands; 3National Museum, UFRJ, Rio de Janeiro, Brazil and 4Coral Vivo Institute, Rio de Janeiro, Brazil Coral reefs are at serious risk due to events associated with global climate change. Elevated ocean temperatures have unpredictable consequences for the ocean’s biogeochemical cycles. The nitrogen cycle is driven by complex microbial transformations, including nitrogen fixation. This study investigated the effects of increased seawater temperature on bacteria able to fix nitrogen (diazotrophs) that live in association with the mussid coral Mussismilia harttii. Consistent increases in diazotroph abundances and diversities were found at increased temperatures. Moreover, gradual shifts in the dominance of particular diazotroph populations occurred as temperature increased, indicating a potential future scenario of climate change. The temperature-sensitive diazotrophs may provide useful bioindicators of the effects of thermal stress on coral reef health, allowing the impact of thermal anomalies to be monitored. In addition, our findings support the development of research on different strategies to improve the fitness of corals during events of thermal stress, such as augmentation with specific diazotrophs. The ISME Journal (2014) 8, 2272–2279; doi:10.1038/ismej.2014.70; published online 16 May 2014 Subject Category: Microbial ecosystem impacts Keywords: climate change; coral reef; nitrogen cycle; Mussismilia harttii; diazotrophs Introduction 2011). Such stresses have already been linked to disease outbreaks in coral reef ecosystems Coral reefs constitute ecosystems that harbor a (Sutherland et al., 2004; Selig et al., 2006). myriad of interwoven species. These ecosystems Corals live in symbiotic relationships with a have key roles in the maintenance of marine plethora of organisms, including endosymbiotic biodiversity. Although coral reefs account for only dinoflagellate algae (zooxanthellae), bacteria, 0.1% of the total ocean area, they host 25% of archaea and fungi (Falkowski et al., 1984; Rohwer all marine macro-organisms that live in the oceans et al., 2002; Knowlton and Rohwer, 2003; Reshef (Burke et al., 2011). Furthermore, they have an et al., 2006). The whole association has been important role in the biogeochemical cycles of described as a holobiont (Rosenberg et al., 2007). carbon, nitrogen and phosphorus that occur in the Intricate relationships may exist between members sea (Wild et al., 2005). Coral reefs are being of the microbial community that occur in the coral threatened by direct anthropogenic impacts as well holobiont. An example is the production as by the effects of global climate change, which may of dimethylsulfoniopropionate by symbiotic zoo- result in a reduction in the pH of seawater and rising xanthellae (Keller et al., 1989), which has been water temperatures (Hoegh-Guldberg et al., 2007; implicated in the prevention of deleterious bacterial Hoegh-Guldberg and Bruno, 2010; Burke et al., colonization of coral. The presence of dimethyl- sulfoniopropionate and related sulfur compounds may provide a selective environment in which the Correspondence: JD van Elsas, Department of Microbial Ecology, survival of microbes is restricted (Barott and Centre for Ecological and Evolutionary Studies, University of Groningen, Groningen, The Netherlands. Rohwer, 2012). Dimethylsulfoniopropionate is a E-mail: [email protected] precursor of the volatile organic sulfur compound or RS Peixoto, General Microbiology, Federal University of Rio de dimethyl sulfide, which may have a role in the Janeiro, Av Carlos Chagas Filho, 373, CCS, Bloco E, Rio de Janeiro formation of clouds and thus acts as a climate- 21 944970, Brazil. E-mail: [email protected] cooling gas (Charlson et al., 1987). On the other Received 20 November 2013; revised 17 March 2014; accepted 23 hand, the growth and abundance of zooxanthellae is March 2014; published online 16 May 2014 limited by the availability of nitrogen (Falkowski Climate change affects coral microbiota HF Santos et al 2273 et al., 1993). In nitrogen-limited coral systems, the and therefore followed natural day/night cycles. To abundance of zooxanthellae may depend on the mimic the amount of incident light in the reefs, the activity of diazotrophic bacteria (Lesser et al., 2007; tanks were covered with a 70% shade screen, Olson et al., 2009; Lema et al., 2012). resulting in 350 mmol photons m À 2 s À 1 at noon, which Recent studies have shown that increases in is consistent with the average parameters measured seawater temperature can cause shifts in the coral- in situ at 2.5 m depth in the ‘Recife de Fora’ reef. associated microbial communities (for example, Five different polyps from four different coral Bourne et al., 2008). However, the effects of outcrops all belonging to the same species, M. harttii temperature increase on the diazotrophic bacterial ( ¼ M. harttii 20 polyps), were collected in the reef populations of corals, and the effect of this on coral area of ‘Recife de Fora’, Brazil. A total of five health, remains unclear. The current study aimed to treatments were evaluated (that is, pretreatment, foster our understanding of the effect of increases control, þ 1.0, þ 2.0 and þ 4.5 1C). One polyp from in seawater temperature on the abundance and each coral outcrop was used in each of the different diversity of diazotrophic microbial populations treatments, thus generating four replicates per associated with the coral Mussismilia harttii. In the treatment. The pretreatment samples were frozen present study, a comparison was made between at À 20 1C immediately after sampling. Polyps mesocosms held at elevated temperatures and subjected to the other treatments were transferred mesocosms maintained at ambient temperatures. to the experimental tanks (o12 h). Polyps in tanks Analysis of nifH genes, which encode the key were kept at natural seawater temperature for dinitrogen reductase enzyme, was used to evaluate acclimation for 15 days. After this period, the tanks the abundance, community structure, species rich- were subjected to the temperature treatments for a ness and diversity of the diazotrophic communities period of 21 days, as follows: ambient water in individual coral specimens from mesocosms temperature (tank control) and three different maintained at different temperatures. An enhanced elevated water temperatures ( þ 1.0, þ 2.0 and understanding of coral-associated nitrogen-fixing þ 4.5 1C) above the ambient temperature. One polyp bacterial communities on coral reefs contributes to from each of the four coral outcrops was used in our understanding of the resilience of coral reefs and each of the five different treatments, thus generating the possible changes in the marine nitrogen cycle in four replicates per treatment. the face of climate change. In addition, it aids in the For quantitative PCR (qPCR), denaturing gradient establishment of potential management guidelines gel electrophoresis (DGGE) analyses, and evaluation for future environmental protection programs. for maximum quantum yield of the Photosystem II (Fv/Fm), all treatments were sampled. For clone Materials and methods library analyses, samples from the following treatments were analyzed: pretreatment, control, Sample collection and experimental design þ 2.0 and þ 4.5 1C. M. harttii specimens were collected in ‘Recife de Fora’, a reef located B3.2 km offshore near the city Photosystem II photochemical efficiency: pulse of Porto Seguro, Bahia, Brazil (between latitude amplitude modulation fluorometry 1612303000S and 1612500600S and longitude Samples were evaluated for maximum quantum 3815803000W and 3815901800W). The reef area is yield of the Photosystem II (Fv/Fm) using B17.5 km2, and the water depth surrounding the a submersible pulse-amplitude-modulated chloro- reef is B20 m. Seawater was sampled at ambient phyll fluorometer (Diving-PAM, Walz, Effeltrich, temperature (B27 1C). Annual temperature fluctua- Germany) as a proxy for the ‘health’ of the coral tion ranged between 24.06 1C (min) and 29.00 1C holobiont (Schreiber, 2004). The measurements (max), and the average water temperature was were taken after sunset in order to avoid interference 26.74 1C(±1.01). The M. harttii colonies had by diurnal photo-inhibition artifacts, after full polyps, which showed loose tissue connection with recovery of the reaction centers. The results were adjacent polyps. Therefore, single- or double-polyp analyzed using a nested analysis of variance with structures were used as sampling units without Statistica 7 software (StatSoft, Tulsa, OK, USA), harming their tissues. Physiological experiments considering the data from four replicate tanks per were conducted in mesocosms established at an treatment and three polyps from three different onshore research station, near the reef area where areas of the reef per tank.
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