View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Sapientia Acidification increases abundances of Vibrionales and Planctomycetia associated to a seaweed-grazer system: potential consequences for disease and prey digestion efficiency Tania Aires1,*, Alexandra Serebryakova1,2,*, Frédérique Viard2,3, Ester A. Serrão1 and Aschwin H. Engelen1 1 Center for Marine Sciences (CCMAR), CIMAR, University of Algarve, Campus de Gambelas, Faro, Portugal 2 Sorbonne Université, CNRS, Lab Adaptation and Diversity in Marine Environments (UMR 7144 CNRS SU), Station Biologique de Roscoff, Roscoff, France 3 CNRS, UMR 7144, Divco Team, Station Biologique de Roscoff, Roscoff, France * These authors contributed equally to this work. ABSTRACT Ocean acidification significantly affects marine organisms in several ways, with complex interactions. Seaweeds might benefit from rising CO2 through increased photosynthesis and carbon acquisition, with subsequent higher growth rates. However, changes in seaweed chemistry due to increased CO2 may change the nutritional quality of tissue for grazers. In addition, organisms live in close association with a diverse microbiota, which can also be influenced by environmental changes, with feedback effects. As gut microbiomes are often linked to diet, changes in seaweed characteristics and associated microbiome can affect the gut microbiome of the grazer, with possible fitness consequences. In this study, we experimentally investigated the effects of acidification on the microbiome of the invasive brown seaweed Sargassum muticum and a native isopod consumer Synisoma nadejda. Both were exposed to ambient CO2 conditions Submitted 13 September 2017 (380 ppm, pH 8.16) and an acidification treatment (1,000 ppm, pH 7.86) for three Accepted 26 January 2018 weeks. Microbiome diversity and composition were determined using high-throughput Published 30 March 2018 sequencing of the variable regions V5-7 of 16S rRNA. We anticipated that as a result Corresponding author of acidification, the seaweed-associated bacterial community would change, leading Aschwin H. Engelen, to further changes in the gut microbiome of grazers. However, no significant effects [email protected] of elevated CO2 on the overall bacterial community structure and composition were Academic editor revealed in the seaweed. In contrast, significant changes were observed in the bacterial Mario Alberto Flores-Valdez community of the grazer gut. Although the bacterial community of S. muticum as Additional Information and whole did not change, Oceanospirillales and Vibrionales (mainly Pseudoalteromonas) Declarations can be found on significantly increased their abundance in acidified conditions. The former, which page 20 uses organic matter compounds as its main source, may have opportunistically taken DOI 10.7717/peerj.4377 advantage of the possible increase of the C/N ratio in the seaweed under acidified Copyright conditions. Pseudoalteromonas, commonly associated to diseased seaweeds, suggesting 2018 Aires et al. that acidification may facilitate opportunistic/pathogenic bacteria. In the gut of S. Distributed under nadejda, the bacterial genus Planctomycetia increased abundance under elevated Creative Commons CC-BY 4.0 CO2. This shift might be associated to changes in food (S. muticum) quality under OPEN ACCESS How to cite this article Aires et al. (2018), Acidification increases abundances of Vibrionales and Planctomycetia associated to a seaweed- grazer system: potential consequences for disease and prey digestion efficiency. PeerJ 6:e4377; DOI 10.7717/peerj.4377 acidification. Planctomycetia are slow-acting decomposers of algal polymers that could be providing the isopod with an elevated algal digestion and availability of inorganic compounds to compensate the shifted C/N ratio under acidification in their food. In conclusion, our results indicate that even after only three weeks of acidified conditions, bacterial communities associated to ungrazed seaweed and to an isopod grazer show specific, differential shifts in associated bacterial community. These have potential consequences for seaweed health (as shown in corals) and isopod food digestion. The observed changes in the gut microbiome of the grazer seem to reflect changes in the seaweed chemistry rather than its microbial composition. Subjects Ecology, Marine Biology, Microbiology, Climate Change Biology, Biological Oceanography Keywords Invasive seaweeds, Ocean acidification, Grazer microbiomes, Algae microbiomes, Metabarcoding, Sargassum muticum, Synisoma nadejda BACKGROUND Ocean acidification significantly affects marine organisms in diverse ways (Fabry et al., 2008; Kroeker et al., 2013). In the case of species interactions (e.g., predator–prey), the outcome of such effects can be difficult to predict as antagonistic or synergistic effects may be observed (Asnaghi et al., 2013; Branch et al., 2013; Poore et al., 2013). This is particularly true for non-calcifying seaweeds, which in contrast to most other organisms can benefit from rising CO2 through increased photosynthesis and carbon acquisition, and subsequently acquire higher growth rates (Porzio, Buia & Hall-Spencer, 2011; Harley et al., 2012; Koch et al., 2013; Olischläger et al., 2013). However, changes in plant leaf chemistry in response to elevated carbon supply are expected to result in higher C:N and C:P ratios and, as such, reduce the nutritional quality of tissue for grazers (Urabe, Togari & Elser, 2003; Van De Waal et al., 2010) and the same is expected for seaweeds. Variations in the palatability of seaweeds may lead to changes in consumption rates by herbivores, which will have to absorb nutrients more efficiently or consume more to compensate for low concentrations of essential nutrients (Gutow et al., 2014). Thus, ocean acidification (OA) could have positive effects on seaweed growth rate, but may also induce behavioral changes on the herbivores and increased grazing rates. Therefore, it is important to understand the effects of ocean acidification on prey (bottom-up effects) and, as a top-down effect, on predation. Interactions among organisms and their associated bacterial communities affect the holobiont physiology and health (Hollants et al., 2013; Egan et al., 2013), and play an important role in the functioning of hosts as, in the case of this study, seaweeds (Singh et al., 2011; Singh & Reddy, 2014). Seaweeds and marine organisms feeding on them live in a close association with diverse and abundant microbial communities (King et al., 2012; Hollants et al., 2013; Egan et al., 2013; Dudek et al., 2014). Seaweeds comprise dynamic species- specific bacterial communities (Aires et al., 2015; Aires, Serrão & Engelen, 2016; Vieira et al., 2016). The communities are recognized to have growth-promoting and nutritional effects (Head & Carpenter, 1975; Dimitrieva, Crawford & Yüksel, 2006), and to be involved Aires et al. (2018), PeerJ, DOI 10.7717/peerj.4377 2/31 in the production of biologically active (Chojnacka et al., 2012) and defensive (Burgess et al., 1999) compounds. At a higher trophic level, symbiotic bacteria inhabiting the guts of marine herbivores are also known to support important physiological functions (Hacquard et al., 2015), including the mediation of the digestion of food components by producing critical digestive enzymes for breaking down complex molecular structures (Mackie et al., 2004). In addition to digestive functions, grazers depend on seaweed-associated microbiota for nutrients found in the algal biofilm (i.e., proteins, polysaccharides, lipids, etc.; Tietjen, 2014). As such, diet represents an important factor in shaping microbial diversity in the intestinal systems of grazers. So, any changes in bacterial composition of the seaweed may result in diet-induced changes in the gut microbiota of grazers that may eventually affect their metabolism, as well as its fitness and biology (Mattila et al., 2014; Tietjen, 2014). Because carbon acquisition is expected to be facilitated for seaweeds at elevated CO2 levels, higher nutrient uptake is anticipated to help obtain other nutrients in the right balance with carbon. Part of these nutrients might be obtained through the microbiome and, therefore, the specific bacteria responsible for such acquisitions (e.g., phosphorous, nitrogen and iron) (Thomas et al., 2008; Burke et al., 2011b) might be positively selected and increase their abundance. Because OA is expected to affect the interactions between marine herbivores and seaweeds through increased consumption of carbon enriched algal tissue (Gutow et al., 2014), the microbiomes of grazers might help with nutrient acquisition. While better understanding of the diversity and functions of associated symbiotic bacteria is needed, few studies have addressed the diversity and composition of gut microbiota of marine grazers (but see Hong et al., 2011; Devine, Pelletreau & Rumpho, 2012; Davis et al., 2013; Dudek et al., 2014). To predict the responses of aquatic organisms to OA, it is necessary to understand responses of the host-associated microbiota to increasing CO2 and reduced pH. Little is known about the responses of associated microbiota to changes in pCO2 (partial pressure of carbon dioxide) including microbial metabolic capabilities or the ability to rapidly shift the host range (Morrow et al., 2015). Also, there is no consensus regarding whether a decrease in pH causes increase (Kerfahi et al., 2014), decrease (Taylor et al., 2014) or no changes (Hassenrück et al., 2016)