Acidification increases abundances of Vibrionales and Planctomycetia associated to a seaweed-grazer system: potential consequences for disease and prey digestion efficiency.

Tania Aires,Aschwin H Engelen,Ester A Serrão,Alexandra Serebryakova,Frédérique Viard

doi:10.7717/peerj.4377

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 (380 ppm, pH 8.16) and an acidification treatment (1,000 ppm, pH 7.86) for three weeks. Microbiome diversity and composition were determined using high-throughput sequencing of the variable regions V5-7 of 16S rRNA. We anticipated that as a result of acidification, the seaweed-associated bacterial community would change, leading to further changes in the gut microbiome of grazers. However, no significant effects of elevated CO2 on the overall bacterial community structure and composition were revealed in the seaweed. In contrast, significant changes were observed in the bacterial community of the grazer gut. Although the bacterial community of S. muticum as whole did not change, Oceanospirillales and Vibrionales (mainly Pseudoalteromonas) significantly increased their abundance in acidified conditions. The former, which uses organic matter compounds as its main source, may have opportunistically taken advantage of the possible increase of the C/N ratio in the seaweed under acidified conditions. Pseudoalteromonas, commonly associated to diseased seaweeds, suggesting that acidification may facilitate opportunistic/pathogenic bacteria. In the gut of S. nadejda, the bacterial genus Planctomycetia increased abundance under elevated CO2. This shift might be associated to changes in food (S. muticum) quality under 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.

Highlights

Ocean acidification significantly affects marine organisms in diverse ways (Fabry et al, 2008; Kroeker et al, 2013)
We experimentally investigated the effects of acidification on the microbiomes of an emblematic invasive seaweed, the brown alga Sargassum muticum, and the gut microbiome of a native isopod consumer, Synisoma nadejda
The responses of bacteria associated with S. muticum and the gut of S. nadejda revealed in this study suggest that worst case acidification scenarios may not greatly affect overall bacterial community composition and diversity, but might affect specific bacterial groups

Summary

Introduction

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 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). It is important to understand the effects of ocean acidification on prey (bottom-up effects) and, as a top-down effect, on predation

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