Abstract
Environmental conditions are known to influence corals and their associated communities of microorganisms. However, our insights into the impacts of seasonal changes in ultraviolet radiation (UVR) on both coral physiology and microbiome remain very limited. To address this challenge, we maintained the coral Acropora muricata shaded from UVR or under ambient UVR levels during two contrasting seasons, i.e. summer and winter, and assessed the impact of UVR on the coral holobiont at each season. To this end, we analysed the physiology (e.g. calcification, protein content, photosynthesis-related parameters) and coral microbiota composition, as well as the abundance and composition of the microbial communities and organic matter contents of the surrounding seawater. Our results show major seasonal effects on coral phenotype: (1) a lower host biomass and photosynthesizing, but fast calcifying phenotype in summer, and (2) a higher host biomass and photosynthesizing, but slow calcifying phenotype in winter. UVR had only a significant impact on Symbiodinium functioning. Specifically, high UVR levels reduced photosynthesis efficiency in summer, but an increase in chlorophyll a content may have compensated for this effect. The coral microbiota, which was variable but generally dominated by Endozoicomonas, was not affected by UVR, but its composition differed between seasons. In contrast, UVR had a major, but differential impact on the seawater microbial communities at both seasons. Particularly in summer, bacteria from the Alteromonadaceae were significantly more abundant (15-fold; up to 75%) in seawater under ambient UVR levels. Overall, our study suggests that UVR has only a limited impact on coral holobiont composition and functioning, despite major fluctuations in the surrounding seawater microbiome; seasonal changes in the holobiont are thus mostly driven by other environmental factors.
Highlights
Population dynamics and reproductive cycles of many species are influenced by seasonal variations in environmental factors (Clarke, 1988; Gooday et al, 1990; Coma et al, 2000), leading to a longstanding interest in the way organisms react to the changing of seasons
Under ambient ultraviolet radiation (UVR) exposure, there was no difference in symbiont density and chlorophyll a content in the tissues of A. muricata between seasons (Table S1, Figures 1A,B,C), but the maximal relative electron transport rate, which is a proxy for the photosynthetic efficiency of the symbionts, was 54% lower in summer compared to winter (Figure 1D)
UVR shading significantly decreased the rETRmax by 29% in winter (Table S1); it was increased by 48% in summer, despite a lower chl a content in the tissues and per Symbiodinium cell
Summary
Population dynamics and reproductive cycles of many species are influenced by seasonal variations in environmental factors (Clarke, 1988; Gooday et al, 1990; Coma et al, 2000), leading to a longstanding interest in the way organisms react to the changing of seasons. Nutrient levels and water quality can vary by a factor 5 between seasons, through for example, sediment loading, or metal and nutrient pollution (Browne et al, 2015; Watson et al, 2017). Seasonality is reflected both in the coral physiology (Crossland, 1984; Warner et al, 2002; Ulstrup et al, 2008) and in the composition of coral-associated microbial communities (Brown et al, 1999; Fitt et al, 2000; Littman et al, 2010; Li et al, 2014). The symbiotic association of the coral animal with its diverse assemblages of microorganisms consisting in bacteria, archaea, fungi, viruses, and protists, including the dinoflagellate algae Symbiodinium (Kelly et al, 2014; Apprill et al, 2016), is termed the coral holobiont (Rohwer et al, 2002)
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