The coral holobiont highlights the dependence of cnidarian animal hosts on their associated microbes

Claudia Pogoreutz, Christian R. Voolstra,

Nils Radecker; Virginia Weis,

Anny Cardenas, and Jean-Baptiste Raina

Introduction: The coral holobiont as an ecosystem engineer and its reliance on associated microbes

The productivity and biodiversity of coral reefs are unmatched in the marine environment (Hatcher 1990). Surrounded by oligotrophic oceans, coral reefs are buzzing oases of life in a marine desert (Darwin 1842). Tropical coral reefs cover just 0.1% of the seafloor but provide habitat for ~32% of all marine multicellular species (Fisher et al. 2015) and contribute to the livelihoods of more than 600 million people (Moberg and Folke 1999; Wilkinson 2008; Spalding et al. 2017). This entire ecosystem is supported by its foundation species: reef-building corals (Figure 7.1). These organisms sustain the immense productivity of coral reefs (Wild et al. 2004), contribute to the reef food web, and their calcareous skeletons form the structural basis of the reef framework.

As early as the 19th century, scientists identified the cohabitation of benthic cnidarians with intracellular photosynthetic dinoflagellates, initially termed “zooxanthellae” (Krueger 2017) (Figure 7.2). Building on more than a century of research, the coral- dinoflagellate symbiosis is one of the best characterized eukaryotic endosymbioses, and a powerful model to understanding the functioning of symbioses in general. Corals also harbor a diverse array of other microbes comprised of protists, fungi, bacteria, archaea, and viruses. This collective is called the coral holobiont (Rohwer et al. 2002). The coral metaorganism, by comparison, is a more restricted definition and typically only describes the coral host and associated microbes for which a function has been proposed or is known (Jaspers et al. 2019). This suite of organisms forms a complex network of symbiotic interactions that extend the metabolic repertoire, immunity, and

Scleractinian corals are the foundation species of coral reef ecosystems

FIGURE 7.1 Scleractinian corals are the foundation species of coral reef ecosystems. Complex symbiotic interactions facilitate nutrient uptake and recycling, thereby enabling corals to thrive in highly oligotrophic environments and to build the structural framework of coral reefs. Image credit: Anna Roik.

Overview and diversity of cnidarian-dinoflagellate symbioses. (a) Reefbuilding or stony coral (Anthozoa, Scleractinia

FIGURE 7.2 Overview and diversity of cnidarian-dinoflagellate symbioses. (a) Reefbuilding or stony coral (Anthozoa, Scleractinia: Acropora humilis); (b) Fire coral, a calcifying hydrocoral (Hydrozoa: Millepora platyphylla)-, (c) Blue Coral, a calcifying “soft” coral (Anthozoa, Octocorallia: Heliopora coerulea)-, (d) upside-down jellyfish (Scyphozoa: Cassiopea sp.). All of these marine cnidarian holobiont systems are intimately engaged in a mutualistic relationship with dinoflagellates of the family Symbiodiniaceae.

environmental adaptation of the coral host (Muscatine 1990; Rosenberg et al. 2007; Ritchie 2012; Radecker et al. 2015; Ziegler et al. 2017, 2019; Robbins et al. 2019). Microbes can therefore be considered fundamental to the ecological success of corals and the reefs they build (Bang et al. 2018).

Reef ecosystems have existed for ~240 million years, but face unprecedented and accelerating decline: the 2015-2017 global coral bleaching event affected 74% of reefs worldwide, and up to half of the coral cover was lost on the Great Barrier Reef alone, the largest reef system in the world (Hughes et al. 2018b). Future predictions for coral reefs are dramatic: even under a 1.5°C warming scenario, it is expected that coral reefs will decline by a further 70%-90%, with larger losses of up to 99% projected to be highly likely under a 2.0°C warming scenario (IPCC 2018). Such trajectories make the understanding of coral holobiont functioning and the contribution of its various microbes critical, not only to comprehend how symbiotic interactions have shaped the most biodiverse marine ecosystem on Earth, but also to help conserve and protect corals and the reefs they build for future generations. In this chapter, we discuss the state of knowledge of coral-microbe interactions and how they shape the ecology, resilience, and adaptation of the coral holobiont.

The coral–Symbiodiniaceae relationship

Symbiodiniaceae: Micro-algal engines of the coral holobiont machinery

The ecological success of the coral-Symbiodiniaceae symbiosis is based on efficient nutrient recycling between host and symbiont (Figure 7.3). The driving force of this bidirectional nutrient exchange ultimately lies in the complementary nutrient limitations of the two symbiotic partners (Shantz et al. 2016; Bang et al. 2018). While the heterotrophic coral host is limited by organic nutrient availability (e.g., glucose), the autotrophic intracellular dinoflagellates are limited by inorganic nutrients (e.g., carbon dioxide or ammonium) (Muscatine et al. 1989; Falkowski et al. 1993; Radecker et al. 2015). These reciprocal metabolic exchanges are governed by the uptake of limiting nutrients and release of excess nutrients by each symbiotic partner (Muscatine 1990; Cunning et al. 2017). Symbiodiniaceae translocate high rates of excess photosynthetically-fixed carbon to the coral host. The host metabolism, in turn, produce w'aste compounds such as carbon dioxide through respiration available to the Symbiodiniaceae (Falkowski et al. 1993). This nutrient exchange is so efficient that the translocation of photosynthates can fully meet or even exceed the respiratory requirements of the coral host (Muscatine and Porter 1977; Muscatine 1990; Falkowski et al. 1993), and hence constitutes its primary energy source (Tremblay et al. 2012). As a consequence, symbiotic coral hosts may overcome their carbon limitation and shift instead towards a nitrogen-limited state (Cunning et al. 2017; Radecker et al. 2018).

In a stable symbiosis, host and symbionts are nitrogen-limited and compete for available environmental ammonium (Pernice et al. 2012). Increasing evidence suggests that this resource competition is critical for maintaining the functioning of the coral-Symbiodiniaceae symbiosis (Cui et al. 2019). Coral hosts use the translocated carbon for ammonium assimilation required for amino acid synthesis (Cui et al. 2019). Consequently, carbon translocation reduces nitrogen availability for the dinoflagellates. The nutrient cycling in the intact symbiosis is thus stabilized by a positive feedback loop: because symbionts translocate carbon, they are nitrogen-limited; and because they are nitrogen-limited, a substantial fraction of photosynthetically fixed carbon cannot be channeled towards their biomass and growth, and is hence released to the host. While this “selfish” interaction between host and symbiont is central to the ecological success of the coral-Symbiodiniaceae relationship, it also renders the symbiosis highly susceptible to environmental disturbance.

Initially considered to be a single species, Symbiodinium microadriaticum (Freudenthal 1962), the recently established family Symbiodiniaceae currently encompasses seven distinct genera (Symbiodinium—formerly Clade A, Breviolum(B), Cladocopium (C), Durusdinium (D), Effrenium (E). Fugacium (F), and Gerakladium (G)) that have originated and diversified alongside reef-building corals approximately 160 mya ago (LaJeunesse et al. 2018). Coral reefs of the Indo-Pacific are almost exclusively dominated by Cladocopium and Durusdinium (LaJeunesse et al. 2003, 2004), with at least 50-100 possible “species” currently identified around Australia alone (LaJeunesse et al. 2003; Silverstein et al., 2011). The remarkable diversity of this family influences their host’s susceptibility to environmental fluctuations, such as thermal stress and salinity (Berkelmans and van Oppen 2006; Sampayo et al.

2008). In the world's warmest reefs of the Persian/Arabian Gulf, corals predominantly harbor Cladocopium thermophilum, an association that is central to the thermotolerance of these coral communities (Hume et al. 2016). Similarly, the stress-tolerant Durusdinium trenchii has rapidly taken over Caribbean corals following repeated anthropogenic disturbances and increasing seawater temperatures (Pettay et al. 2015). However, thermal adaptation of reef communities represents a significant physiological tradeoff: corals harboring D. trenchii typically grow slower (Little et al. 2004) and incorporate only half the amount of photosynthates compared to those associated with Cladocopium (Cantin et al. 2009). Recently, multiple Symbiodiniaceae genomes have become available (Shoguchi et al. 2013; Lin et al. 2015; Aranda et al. 2016), and comparative analyses have revealed that these organisms possess an extensive transporter repertoire for carbon and nitrogen metabolites, which is unique among dinoflagellates and likely underpins their symbiotic lifestyle (Aranda et al. 2016).

Innate immunity, symbiosis sensing, and cell signaling

The regulation of the coral-Symbiodiniaceae partnership is complex and only partially understood. There is strong evidence that the host innate immune system plays a large role in mechanisms of recognition, maintenance, and dysbiosis of the association (Weis 2008). In the majority of coral species, the symbiosis is established anew with each host generation. The algae are acquired via phagocytosis by nutritive phagocytes that comprise the host gastrodermal tissue (endoderm) (Fadlallah 1983). However, instead of being digested, the algae specific to a particular host persist and proliferate within host vacuoles (termed symbiosomes) (Colley and Trench 1983; Schwarz et al. 1999). This process is mediated by the host innate immune system (Palmer 2018). The process of phagocytosis is a complex part of innate immunity that is highly conserved across the Metazoa (Underhill and Ozinsky 2002).

Microbes, including Symbiodiniaceae, are arrayed with a variety of microbe- associated molecular patterns (MAMPs), including glycans, that are recognized by host pattern recognition receptors (PRRs) on phagocyte cell surfaces (Weis 2008). These MAMP-PRR interactions launch a variety of signaling cascades that determine the fate of the phagocytized microbe. The model in corals is that tolerogenic pathways allow for the persistence and proliferation of algal symbionts inside symbiosomes, while resistant pathways are launched during dysbiosis and bleaching (see next section) that reject and remove the symbiont. There is overwhelming evidence for the presence of MAMP-PRR interactions and downstream innate immune signaling in corals. The majority of evidence comes from now extensive -omics studies that repeatedly point to elaboration, enhancement, and overexpression of innate immunity genes in corals and other symbiotic cnidarians (Rodriguez-Lanetty et al. 2004; Shinzato et al. 2011; Baumgarten et al. 2015; Mohamed et al. 2016; Voolstra et al. 2017; Cunning et al. 2018; Shumaker et al. 2019). There are also a variety of studies, often in sea anemone model systems, that provide evidence of innate immune pathway function including: host lectin-symbiont glycan interactions (Wood-Charlson et al. 2006; Bay et al. 2011; Parkinson et al. 2018), scavenger receptors (Neubauer et al. 2016), thrombospondin type 1 repeat proteins (Wolfowicz et al. 2016; Neubauer et al. 2017), complement system (Poole et al. 2016), the master immunity gatekeeper NF-кВ (Mansfield et al.

2017), tolerogenic TGF(3 pathway (Detournay et al. 2012; Berthelier et al. 2017), sphingolipid signaling (Kitchen and Weis 2017; Kitchen et al. 2017), and Rab protein signaling and other evidence of endosomal trafficking (Chen et al. 2003, 2004).

Also critical to symbiosis regulation is the maintenance of host and symbiont biomass ratios through cell cycle regulation. Host and symbiont biomass ratios reach a dynamic homeostasis after symbionts fully colonize a host (Davy et al. 2012). Symbiont populations in hospite grow much more slowly than those in culture and are arrested at the Gl/S transition (Smith and Muscatine 1999). Mechanisms that coordinate the two cell cycles and an understanding of how this coregulation becomes decoupled during dysbiosis have yet to be revealed.

Coral bleaching: The breakdown of the coral–Symbiodiniaceae relationship

Stressful environmental conditions such as temperature anomalies, nutrient enrichment, or pollution can result in so-called coral bleaching, a (general) stress response characterized by whitening of the coral tissue caused primarily by the loss of Symbiodiniaceae endosymbionts from the tissue via expulsion, host cell apoptosis/ detachment, digestion, orexocytosis of the symbiont cells (Gates et al. 1992; Douglas 2003; Dunn et al. 2007; Davy et al. 2012). Coral bleaching can also occur via the loss of photosynthetic pigment from the symbionts in hospite (Jones et al. 1998). Several triggers that induce the coral bleaching cascade have been proposed, including oxidative stress (Lesser 1997) and changes in nutrient stoichiometry (Wiedenmann et al. 2012; Morris et al. 2019). However, the underlying cellular mechanisms are still not fully understood.

Corals may recover from a bleaching event by repopulating their tissues with Symbiodiniaceae (Jones et al. 2008; Silverstein et al. 2015). However, as bleaching effectively results in the disruption of carbon fixation by Symbiodiniaceae and subsequent loss of photosynthate translocation to the coral host (Ezzat et al. 2015), coral host starvation may eventually result in mortality as a consequence of prolonged bleaching. The availability of heterotrophic food sources and the heterotrophic capacity of the host, thus, may determine the resilience of corals during heat stress (Grottoli et al. 2006). Mass coral bleaching events at the ecosystem scale have resulted in the loss of entire reefs, or reef systems (Hoegh-Guldberg 2011; Hughes et al. 2018a) and are projected to increase in the future due to climate change driving ocean warming (IPCC 2018).

The majority of contemporary observations of ecosystem-scale coral bleaching coincide with high-temperature anomalies, such as the El Nino Southern Oscillation (ENSO), or marine heatwaves, which can push corals beyond their thermal limits (Hoegh-Guldberg 1999; Hughes et al. 2003, 2017, 2018a). The first observations of coral bleaching were made in 1983 in the Eastern Pacific near the Panama-Costa Rica border (Glynn 1983). Due to the increasing severity and frequency of high-temperature anomalies attributed to global warming, coral bleaching events have become more common in the past decades. Since then, three mass bleaching events have occurred at the global scale, subsequently named the First, Second, and Third Global Bleaching Event, recorded in 1997/1998,2009/2010, and 2015-2016, respectively (Hughes et al.

2017). A recent analysis of bleaching records of 100 reefs from 1980-2016 has shown that the average turnaround time between bleaching events has halved in the past thirty years and is now only six years (Hughes et al. 2018a). This concerning trend means that the likelihood of recurring annual mass bleaching events in the coming decade is increasing, and the amount of time in between these bleaching events is no longer sufficient to allow full reef recovery (Hughes et al. 2018a).

 
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