Microbes in the coral holobiont: partners through evolution, development, and ecological interactions

Abstract

In the last two decades, genetic and genomic studies have revealed the astonishing diversity and ubiquity of microorganisms. Emergence and expansion of the human microbiome project has reshaped our thinking about how microbes control host health-not only as pathogens, but also as symbionts. In coral reef environments, scientists have begun to examine the role that microorganisms play in coral life history. Herein, we review the current literature on coral-microbe interactions within the context of their role in evolution, development, and ecology. We ask the following questions, first posed by McFall-Ngai et al. (2013) in their review of animal evolution, with specific attention to how coral-microbial interactions may be affected under future environmental conditions: (1) How do corals and their microbiome affect each other's genomes? (2) How does coral development depend on microbial partners? (3) How is homeostasis maintained between corals and their microbial symbionts? (4) How can ecological approaches deepen our understanding of the multiple levels of coral-microbial interactions? Elucidating the role that microorganisms play in the structure and function of the holobiont is essential for understanding how corals maintain homeostasis and acclimate to changing environmental conditions.

Keywords: bacterial interactions; biological; coral; ecosystem; holobiont; metamorphosis; pollution and global change; symbiosis.

Figure 1

Coral reproductive cycle. Spawning corals (shown as branching) release gamete bundles, eggs, or sperm, and brooding corals (shown as massive) release planulae. Inset (A) shows close up of gamete bundle. Inset (B) shows close up of planula larva.

Figure 2

Anatomy of coral polyp. Basal body wall not shown. Inset (A), shows close up of mucus layer, epidermis and upper gastrodermis. Inset (B), shows close up of coral gastrovascular cavity.

Figure 3

Oxygen profile in the gastrovascular cavity of a coral polyp adapted from averaged data presented in Agostini et al. (2012).

Figure 4

Conceptual model of top and bottom down control of the microbiota structure in the coral holobiont. Stable microbes may be introduced to the holobiont through horizontal or vertical transmission and persist in ecological niches within the coral polyp where growth (or immigration) rates balance removal pressures from biophysical processes and immune or ecological interactions. Transient microbes enter the holobiont from environmental sources (e.g., seawater, prey items, or suspension feeding) and removal rates exceed growth/immigration rates such that a dynamic and high diversity microbiota results. Transient and stable populations compete for resources including nutrients, light and space and the outcome of resource-based competition (bottom up control) ultimately determines population growth rate and thus ability to persist when subject to removal. Whether a population is categorized as stable or transient may depend on the timeframe considered. Abbreviations: AMP, antimicrobial peptides; ROS, reactive oxygen species.

Figure 5

Trophic connections of the coral holobiont in the planktonic food web.