How Does the Coral Microbiome Cause, Respond to, or Modulate the Bleaching Process?

Abstract

Coral holobionts are formed by a dynamic multipartite symbiosis with intracellular photoautotrophs in the genus Symbiodinium, as well as a consortium of microor- ganisms that include bacteria, archaea, viruses, fungi, and protists. The coral holobiont functions as a unit to provide flexible stability in the face of constant environmental stressors. Coral bleaching, or the loss of Symbiodinium and their pigments, has caused significant global declines in the percentage cover of reef- building corals, particularly in recent decades as global sea surface temperatures continue to rise (Lesser 2004; Hoegh-Guldberg et al. 2007). Bleaching can be caused by a number of environmental stressors including extreme fluctuations in seawater temperature (increase or decrease), high solar irradiance, sedimentation, pollution, herbicides, and reduced salinity. Hyperoxic conditions have been shown to act synergistically with solar radiation and thermal stress to produce significantly greater fluxes of reactive oxygen species (ROS) in both host tissues and Symbiodinium spp. that leads to photosynthetic dysfunction, apoptosis, and bleaching (Lesser 2006, 2011; Oakley et al. 2017). We now understand that different phylotypes of Symbiodinium sp. within each clade represent multiple phenotypes and potentially species (Thornhill et al. 2014), and display variable rates of photosynthesis, capacity to photoacclimate, stress tolerance, ROS production, superoxide dismutase (SOD) activity, and metabolic interchange with their hosts (Banaszak et al. 2006; Robison and Warner 2006; Reynolds et al. 2008; Suggett et al. 2008; Hennige et al. 2009; Brading et al. 2011; Lesser 2011; Buxton et al. 2012; McGinty et al. 2012; Parkinson and Baums 2014; Roberty et al. 2014; Krueger et al. 2015; Warner and Suggett 2016; Grégoire et al. 2017). However, much less attention has been paid to the coral microbiome, which includes the Symbiodinium, prokaryotes and viruses, and their role in coral bleaching and the bleaching response. Microbes can exhibit extensive diversity and abilities to respond to and withstand environmental pressures, and, as with other multipartite mutualisms (Hussa and Goodrich-Blair 2013), corals may be able to take advantage of these microbial partnerships by recruiting taxa with distinct environmental toler- ances that provide a means to adapt and/or acclimate to environmental change. Here, we provide some context for the importance of the coral microbiome to holobiont function. We survey what is currently known about the relationship among Symbiodinium, temperature stress, and the associated prokaryotes and viruses. We also examine the impact of the coral bleaching response and environmental stressors conducive to bleaching (e.g., temperature and irradiance) on coral-associated micro- organisms with particular emphasis on diazotrophic (nitrogen-fixing) bacteria. In conclusion, we summarize how a shifting and potentially dysbiotic microbiome may impact the coral host in the context of bleaching.