Microbial contributions to the persistence of coral reefs

Abstract

On contemplating the adaptive capacity of reef organisms to a rapidly changing environment, the microbiome offers significant and greatly unrecognised potential. Microbial symbionts contribute to the physiology, development, immunity and behaviour of their hosts, and can respond very rapidly to changing environmental conditions, providing a powerful mechanism for acclimatisation and also possibly rapid evolution of coral reef holobionts. Environmentally acquired fluctuations in the microbiome can have significant functional consequences for the holobiont phenotype upon which selection can act. Environmentally induced changes in microbial abundance may be analogous to host gene duplication, symbiont switching / shuffling as a result of environmental change can either remove or introduce raw genetic material into the holobiont; and horizontal gene transfer can facilitate rapid evolution within microbial strains. Vertical transmission of symbionts is a key feature of many reef holobionts and this would enable environmentally acquired microbial traits to be faithfully passed to future generations, ultimately facilitating microbiome-mediated transgenerational acclimatisation (MMTA) and potentially even adaptation of reef species in a rapidly changing climate. In this commentary, we highlight the capacity and mechanisms for MMTA in reef species, propose a modified Price equation as a framework for assessing MMTA and recommend future areas of research to better understand how microorganisms contribute to the transgenerational acclimatisation of reef organisms, which is essential if we are to reliably predict the consequences of global change for reef ecosystems.

Figure 1

Conceptual overview of the microbial mechanisms facilitating transgenerational acclimatisation of coral reef organisms. Under elevated seawater temperature and pCO₂, specific host-associated microorganisms may increase or decrease in abundance, thereby altering holobiont function and fitness. These frequency shifts can occur in the Symbiodinium (large circular cells differentially shaded according to clade) or prokaryotic community (rod-shaped cells). Shifts in community composition can also occur via acquisition of new microorganisms from the surrounding environment. In addition, mutation and/or horizontal gene transfer can introduce new genetic material into existing symbiont populations (white cells with black inset). This process can occur in any component (Symbiodinium, bacteria, archaea) of the host microbiome. If microbial alterations that infer a fitness advantage to the host are vertically transmitted to the offspring (denoted by sketch of a newly settled coral recruit), transgenerational acclimatisation can occur.