Towards enhancing coral heat tolerance: a “microbiome transplantation” treatment using inoculations of homogenized coral tissues

Abstract

Background Microbiome manipulation could enhance heat tolerance and help corals survive the pressures of ocean warming. We conducted coral microbiome transplantation (CMT) experiments using the reef-building corals, Pocillopora and Porites, and investigated whether this technique can benefit coral heat resistance while modifying the bacterial microbiome. Initially, heat-tolerant donors were identified in the wild. We then used fresh homogenates made from coral donor tissues to inoculate conspecific, heat-susceptible recipients and documented their bleaching responses and microbiomes by 16S rRNA gene metabarcoding. Results Recipients of both coral species bleached at lower rates compared to the control group when exposed to short-term heat stress (34 °C). One hundred twelve (Pocillopora sp.) and sixteen (Porites sp.) donor-specific bacterial species were identified in the microbiomes of recipients indicating transmission of bacteria. The amplicon sequence variants of the majority of these transmitted bacteria belonged to known, putatively symbiotic bacterial taxa of corals and were linked to the observed beneficial effect on the coral stress response. Microbiome dynamics in our experiments support the notion that microbiome community evenness and dominance of one or few bacterial species, rather than host-species identity, were drivers for microbiome stability in a holobiont context. Conclusions Our results suggest that coral recipients likely favor the uptake of putative bacterial symbionts, recommending to include these taxonomic groups in future coral probiotics screening efforts. Our study suggests a scenario where these donor-specific bacterial symbionts might have been more efficient in supporting the recipients to resist heat stress compared to the native symbionts present in the control group. These findings urgently call for further experimental investigation of the mechanisms of action underlying the beneficial effect of CMT and for field-based long-term studies testing the persistence of the effect.

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

“…The composition of bacterial assemblages associated with corals is rarely static and often displays seasonal ( Roder et al, 2015 ; Sharp et al, 2017 ) and spatial ( McDevitt-Irwin et al, 2017 ; Ziegler et al, 2019 ; Osman et al, 2020 ) heterogeneity governed by changing environmental conditions. There is evidence that these bacterial communities can also facilitate coral acclimation under environmental stress, enhancing coral resilience ( Ziegler et al, 2017 , 2019 ; Yu et al, 2020 ), and recent microbiome manipulation experiments have led to altered levels of stress susceptibility ( Fragoso Ados Santos et al, 2015 ; Damjanovic et al, 2017 ; Rosado et al, 2019 ; Doering et al, 2021 ; Zhang et al, 2021 ). However, the specific metabolic advantages that beneficial bacteria provide to corals remain to be elucidated.…”

Microbiome Structuring Within a Coral Colony and Along a Sedimentation Gradient

“…Another ASV which belongs to the genus Peredibacter was differentially abundant across the sedimentation gradient for both edge and sediment samples. This ASV was also more abundant closest to the river mouth and is part of a genus classified as a predatory, Gramnegative, bacteriovorus group ubiquitous in soil and sewage (Davidov and Jurkevitch, 2004) that has previously been found in association with Pocillopora coral hosts (Doering et al, 2021). In edge samples, two other bacteriovorus ASVs-Pirellula and Rhodopirellula-were also in their greatest abundance at sites by the river mouth.…”

“…In edge samples, two other bacteriovorus ASVs-Pirellula and Rhodopirellula-were also in their greatest abundance at sites by the river mouth. The presence of these three bacteriovores in greater abundance near the river mouth at the edge of colonies might be significant as micropredators can drive microbiome changes in corals even at low abundances (Doering et al, 2021).…”

Horizon scan of rapidly advancing coral restoration approaches for 21st century reef management

“…[65]), prompting interest in developing bacterial probiotics to offset the negative impact of transient heat stress on coral health [66]. Inoculation of corals with cultured bacteria or whole microbiomes isolated from healthy coral can modify the coral-associated bacterial communities, although changes may not be temporally stable [67][68][69][70]. In recent experiments, inoculation with a bacterial cocktail consisting of a small number of strains [68,70] or a microbiome transplant [69] lowered heat stress susceptibility relative to no-inoculum controls.…”