Symbiont shuffling across environmental gradients aligns with changes in carbon uptake and translocation in the reef-building coral Pocillopora acuta

Abstract

Symbiosis between reef-building corals and unicellular algae (Symbiodiniaceae) fuels the growth and productivity of corals reefs. Capacity for Symbiodiniaceae to fix inorganic carbon (Ci) and translocate carbon compounds to the host is central to coral health, but how these processes change for corals thriving in environmental extremes remains largely unresolved. We investigate how a model coral -Pocillopora acuta -persists from a reef habitat into an adjacent extreme mangrove lagoon on the Great Barrier Reef. We combine respirometry and photophysiology measurements, Symbiodiniaceae genotyping, and 13 C labelling to compare P. acuta metabolic performance across habitats, in relation to the Ci uptake and 27 translocation capacity by symbionts' autotrophy. We show that differences in P. acuta 28 metabolic strategies across habitats align with a shift in dominant host-associated 29 Symbiodiniaceae taxon, from Cladocopium in the reef to Durusdinium in the mangroves. This 30 shift corresponded with a change in 'photosynthetic strategy', with P. acuta in the mangroves 31 utilising absorbed light for photochemistry over non-photochemical quenching. Mangrove 32 corals translocated similar proportions of carbon compared to the reefs, despite a lower Ci uptake. These trends indicate that coral survival in mangrove environments occurs through sustained translocation rate of organic compounds from coral symbionts to host. Introduction 36The ecological success of reef-building corals resides on their ability to establish and 37 maintain metabolic exchanges through an effective symbiotic association with dinoflagellates 38 from the family Symbiodiniaceae. Symbiodiniaceae fuel their hosts with organic carbon by fixing inorganic carbon (Ci) through photosynthesis (Davy et al. 2012). While Ci uptake rates by the algal symbionts have rarely been measured, they appear strongly regulated by environmental factors, such as availability of CO2 (pCO2) (Suggett et al. 2012b; Brading et al. 42 2013) and temperature (Oakley et al. 2014). Recent work on cultured Symbiodiniaceae 43 revealed that different environmental optima primarily drive variation in Ci uptake rates (Ros 44 et al. 2020). Within reef systems where Symbiodiniaceae are hosted within cnidarian tissues, symbiont cells are typically carbon-limited (Smith and Muscatine 1999; Doherty 2009; Towanda and Thuesen 2012); as such, cnidarians can exhibit a stimulated carbon metabolism under naturally higher pCO2 (more acidic) environments (Suggett et al. 2012b). The efficiency 48 of Symbiodiniaceae carbon metabolism across environments thus appears an important trait in 49 supporting their host's survival, and a means to cope with stressful conditions. 50 51 Associations between the cnidarian host and specific genera, species or strains of 52 Symbiodiniaceae profoundly influence the stress resilience of their coral host (Berkelmans and 53

Rapid Shifts in Bacterial Communities and Homogeneity of Symbiodiniaceae in Colonies of Pocillopora acuta Transplanted Between Reef and Mangrove Environments

“…Symbiodiniaceae taxa profoundly influence the physiology and stress resilience of their coral hosts ( Oliver and Palumbi, 2011 ; Howells et al, 2012 ; Suggett et al, 2017 ). We found distinct communities of Symbiodiniaceae associated with P. acuta between the reef and mangrove environments, which is in line with previous observations at this field site ( Ros et al, 2021 ). P. acuta colonies on the reef were largely dominated by the genus Cladocopium , whereas the mangrove colonies were dominated by the genus Durusdinium.…”

“…distinct communities of Symbiodiniaceae associated with P. acuta between the reef and mangrove environments, which is in line with previous observations at this field site (Ros et al, 2021). P. acuta colonies on the reef were largely dominated by the genus Cladocopium, whereas the mangrove colonies were dominated by the genus Durusdinium.…”

“…Following recent observations that coral species found on the northern Great Barrier Reef in both mangrove lagoon and adjacent reef sites are inhabited by different communities of Symbiodiniaceae (Low Isles; Camp et al, 2019;Ros et al, 2021), we conducted a 9-month reciprocal transplant experiment, using the common coral species Pocillopora acuta, to identify whether: (i) bacterial communities differ between sites, and (ii) bacterial and Symbiodiniaceae community composition changes to resemble that of native corals when moved across the contrasting environments. Given previous observations of rapid adjustments in bacterial assemblages (Sharp et al, 2017;Sweet et al, 2017;Pootakham et al, 2019), we hypothesised that the microbiome of P. acuta would shift after 9 months of reciprocal transplantation into non-native sites and would mirror that of native non-transplanted corals.…”

“…These environments are also on average 2°C warmer than nearby reefs and contain lower dissolved O 2 concentrations (<1 mg L –1 ) relative to adjacent reefs ( Camp et al, 2017 , 2020 ). As a result, corals thriving in mangrove lagoons exhibit very different physiological and metabolic signatures, such as enhanced respiration and reduced photosynthesis ( Camp et al, 2017 ; Ros et al, 2021 ), which likely facilitate their survival within these relatively hostile environments. However, other underlying factors, such as shifts in the coral microbiome, might also contribute to the persistence of corals in these extreme environments.…”

Reef location has a greater impact than coral bleaching severity on the microbiome of Pocillopora acuta

“…For instance, it is welldocumented that different coral colonies of a given species, exposed to similar levels of thermal stress at the same location can exhibit varying degrees of bleaching (Swain et al 2016;Green et al 2019); however, we do not know if this mosaic of bleaching phenotypes observed at the colony-level is reflected in the microbiome. To address this question, we used the emerging model species Pocillopora acuta, a reef-building coral with well characterised ecology, reproduction and microbiome (Torda et al 2013a;Schmidt-Roach et al 2014a, b;Nakajima et al 2018;Damjanovic et al 2020b;Ros et al 2021). Previous studies have revealed that the microbiomes of Pocillopora species are generally stable under changing environmental conditions (Pogoreutz et al 2018;Epstein et al 2019), with species such as P. acuta often hosting site-specific microbiomes (Torres et al 2020), perhaps due to the brooding reproductive strategy of the host (Torda et al 2013a).…”