Zoantharian Endosymbiont Community Dynamics During a Stress Event

Abstract

Coral reefs are complex ecosystems composed of many interacting species. One ecologically important group consists of zoantharians, which are closely related to reef-building corals. Like corals, zoantharians form mutualistic symbioses with dinoflagellate micro-algae (family Symbiodiniaceae), but their associations remain underexplored. To examine the degree to which zoantharians exhibit altered symbiont dynamics under changing environmental conditions, we reciprocally transplanted colonies of Zoanthus sansibaricus between intertidal (2 m) and subtidal (26 m) depths within a reef in Okinawa, Japan. At this location, Z. sansibaricus can associate with three Symbiodiniaceae species from two genera distributed along a light and depth gradient. We developed species-specific molecular assays and sampled colonies pre- and post-transplantation to analyze symbiont community diversity. Despite large environmental differences across depths, we detected few symbiont compositional changes resulting from transplantation stress. Colonies sourced from the intertidal zone associated with mixtures of a "shallow" Symbiodinium sp. and a "shallow" Cladocopium sp. independent of whether they were transplanted to shallow or deep waters. Colonies sourced from the subtidal zone were dominated by a "deep" Cladocopium sp. regardless of transplant depth. Subtidal colonies brought to shallow depths did not transition to the presumably high-light adapted shallow symbionts present in the new environment, but rather bleached and died. These patterns mirror observations of highly stable coral-algal associations subjected to depth transplantation. Our results indicate that Zoanthus-Symbiodiniaceae symbioses remain stable despite stress, suggesting these important reef community members have relatively low capacity to shuffle to more stress-tolerant micro-algae in response to ongoing climate change.

Keywords: Symbiodiniaceae; Zoanthus sansibaricus; light intensity; quantitative PCR; reciprocal transplant.

Figure 1

Reciprocal transplant design. The first letter of each treatment indicates depth of origin, while the second indicates depth of transplantation. “S” corresponds to “shallow” (intertidal; 2 m); “D” corresponds to “deep” (subtidal; 26 m).

Figure 2

Hourly light (illuminance) and temperature readings at two depths in Manza, Okinawa Island, Japan, averaged over 2 weeks in Summer 2015. “Shallow” corresponds to the intertidal (2 m); “deep” corresponds to the subtidal (26 m). The gray horizontal line indicates zero illuminance. The large error bars for shallow depth reflect high hourly variation in these metrics, as expected in the intertidal zone.

Figure 3

Zoanthus sansibaricus colony mortality over the course of the 2-month reciprocal transplant experiment at Manza in Summer 2013. “W” corresponds to the week of observation. Note the rapid mortality in the deep-to-shallow (DS) transplant, necessitating early sampling to characterize symbiont community composition. Anecdotally, all the living DS colonies were visually bleached at 1 and 2 W.

Figure 4

Consensus cladograms of the noncoding region of the chloroplast psbA minicircle (psbA^ncr) sequences for Symbiodinium spp. (left) and Cladocopium spp. (right) based on distance methodology. Node values indicate bootstrap support (values below 60% excluded). Values correspond to different analyses in the following order: distance/parsimony/maximum likelihood. Dashes indicate where nodes were not supported by the given method.

Figure 5

Changes in Symbiodiniaceae community composition for individual Z. sansibaricus colonies over the course of the reciprocal transplant experiment based on species-specific quantitative PCR (qPCR) during Summer 2013. “W” corresponds to the week of observation. Note that in the DS transplant, the final symbiont community characterization was made at 1 W instead of 4 W due to the onset of rapid mortality and visual bleaching among these colonies. Designations above barplots indicate transplant treatment (two letters) and colony ID (two numbers).

Figure 6

Spatial differences in Symbiodiniaceae community composition across the surfaces of four intertidal Z. sansibaricus colonies collected from Manza’s intertidal zone (2 m) in Spring 2017. Each colony was sampled at five points, represented by the pie charts of proportional abundance for each symbiont species. The gradients are subjective interpretations of symbiont distributions inferred from these points.