Elevated seawater temperature causes a microbial shift on crustose coralline algae with implications for the recruitment of coral larvae

Abstract

Crustose coralline algae (CCA) are key reef-building primary producers that are known to induce the metamorphosis and recruitment of many species of coral larvae. Reef biofilms (particularly microorganisms associated with CCA) are also important as settlement cues for a variety of marine invertebrates, including corals. If rising sea surface temperatures (SSTs) affect CCA and/or their associated biofilms, this may in turn affect recruitment on coral reefs. Herein, we report that the CCA Neogoniolithon fosliei, and its associated microbial communities do not tolerate SSTs of 32 °C, only 2-4 °C above the mean maximum annual SST. After 7 days at 32 °C, the CCA exhibited clear signs of stress, including bleaching, a reduction in maximum quantum yield (F(v)/F(m)) and a large shift in microbial community structure. This shift at 32 °C involved an increase in Bacteroidetes and a reduction in Alphaproteobacteria, including the loss of the primary strain (with high-sequence similarity to a described coral symbiont). A recovery in F(v)/F(m) was observed in CCA exposed to 31 °C following 7 days of recovery (at 27 °C); however, CCA exposed to 32 °C did not recover during this time as evidenced by the rapid growth of endolithic green algae. A 50% reduction in the ability of N. fosliei to induce coral larval metamorphosis at 32 °C accompanied the changes in microbiology, pigmentation and photophysiology of the CCA. This is the first experimental evidence to demonstrate how thermal stress influences microbial associations on CCA with subsequent downstream impacts on coral recruitment, which is critical for reef regeneration and recovery from climate-related mortality events.

Figure 1

Photographic panel of CCA after 7 days at each of the experimental temperature treatments showing loss of pigment at 31 °C and complete bleaching at 32 °C.

Figure 2

Maximum potential quantum yield (F_v/F_m) of CCA in each temperature treatment during the 7 days exposure and subsequent 7 days recovery period.

Figure 3

Percent metamorphosis of coral larvae on CCA that had been treated at 27 °C, 29 °C, 31 °C and 32 °C for 7 days.

Figure 4

Principal components analysis of CCA bacterial community composition at each of the temperature treatments. DGGE banding pattern data generated with rpoB gene primers was used to construct a similarity matrix.

Figure 5

Phyla and class-level differences in bacterial biofilm composition on CCA (a) and reef sediment (b) at each temperature treatment. The ‘other' category contains sequences from the Chloroflexi, Nitrospira and Actinobacteria phyla. Graphs were constructed using the frequency of 16s rRNA sequences belonging to each bacterial group from clone library analysis.

Figure 6

OTU heat maps generated with a distance of 0.03 for CCA (a) and sediment (b) libraries. The 7-day 32 °C CCA library is a distinct outlier and there is greater variability between the CCA derived libraries than the sediment-derived libraries.

Figure 7

Community tree constructed from an OTU assignment using a distance of 0.03. The cluster analysis shows similarity between each of the CCA-derived 16S rRNA gene clone libraries.

Figure 8

Principal components analysis of CCA bacterial community composition at each of the temperature treatments. DGGE banding pattern data generated with primers specific to the Alphaproteobacteria and Bacteroidetes groups.