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

Thompson JR, Rivera HE, Closek CJ, Medina M - Front Cell Infect Microbiol (2015)

Bottom Line: (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.

View Article: PubMed Central - PubMed

Affiliation: Civil and Environmental Engineering Department, Massachusetts Institute of Technology Cambridge, MA, USA.

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.

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Trophic connections of the coral holobiont in the planktonic food web.
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Figure 5: Trophic connections of the coral holobiont in the planktonic food web.

Mentions: In addition to predation and suspension feeding, corals may obtain nutrients directly. Scleractinian corals are capable of uptaking amino acids (Drew Ferrier, 1991; Al-Moghrabi et al., 1993; Grover et al., 2008; Tremblay et al., 2012), ammonium (Burris, 1983), and dissolved and particulate organic matter from the surrounding seawater (Sorokin, 1973; Tremblay et al., 2012). Indeed, 32P-radiolabeling experiments with bacteria or inorganic phosphate demonstrate that six coral species assimilate phosphate directly from seawater, or as labeled bacterioplankton via suspension feeding, with higher efficiency for the latter (Sorokin, 1973). The reverse was true for carbon uptake where 14C-radiolabelled low molecular weight dissolved organic matter (DOM) was taken up more efficiently that the carbon-equivalent of bacterial cells (Sorokin, 1973). Microbes are well-established as agents that enable the transfer of DOM to higher trophic levels through the microbial loop (Azam et al., 1983; Azam and Cho, 1987). Assimilation of DOM into the coral holobiont may also be converted to animal biomass and mucus that is accessible to higher trophic levels (Wild et al., 2004; Naumann et al., 2010). Recently uptake of DOM and conversion to detritus by the sponge holobiont has been shown to play a major role in recycling nutrients in reef ecosystems via a cycle termed the “sponge loop” (de Goeij et al., 2013). Although photosynthetic activity by Symbiodinium in the coral holobiont places corals as net exporters of DOM into reef ecosystems (Wild et al., 2004), uptake of some forms of DOM by the coral holobiont contributes to efficient recycling of fixed carbon and nutrients on reef ecosystems that allows dense assemblages to thrive in nutrient poor regions (e.g., a “coral loop”) (Figure 5).


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

Thompson JR, Rivera HE, Closek CJ, Medina M - Front Cell Infect Microbiol (2015)

Trophic connections of the coral holobiont in the planktonic food web.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4286716&req=5

Figure 5: Trophic connections of the coral holobiont in the planktonic food web.
Mentions: In addition to predation and suspension feeding, corals may obtain nutrients directly. Scleractinian corals are capable of uptaking amino acids (Drew Ferrier, 1991; Al-Moghrabi et al., 1993; Grover et al., 2008; Tremblay et al., 2012), ammonium (Burris, 1983), and dissolved and particulate organic matter from the surrounding seawater (Sorokin, 1973; Tremblay et al., 2012). Indeed, 32P-radiolabeling experiments with bacteria or inorganic phosphate demonstrate that six coral species assimilate phosphate directly from seawater, or as labeled bacterioplankton via suspension feeding, with higher efficiency for the latter (Sorokin, 1973). The reverse was true for carbon uptake where 14C-radiolabelled low molecular weight dissolved organic matter (DOM) was taken up more efficiently that the carbon-equivalent of bacterial cells (Sorokin, 1973). Microbes are well-established as agents that enable the transfer of DOM to higher trophic levels through the microbial loop (Azam et al., 1983; Azam and Cho, 1987). Assimilation of DOM into the coral holobiont may also be converted to animal biomass and mucus that is accessible to higher trophic levels (Wild et al., 2004; Naumann et al., 2010). Recently uptake of DOM and conversion to detritus by the sponge holobiont has been shown to play a major role in recycling nutrients in reef ecosystems via a cycle termed the “sponge loop” (de Goeij et al., 2013). Although photosynthetic activity by Symbiodinium in the coral holobiont places corals as net exporters of DOM into reef ecosystems (Wild et al., 2004), uptake of some forms of DOM by the coral holobiont contributes to efficient recycling of fixed carbon and nutrients on reef ecosystems that allows dense assemblages to thrive in nutrient poor regions (e.g., a “coral loop”) (Figure 5).

Bottom Line: (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.

View Article: PubMed Central - PubMed

Affiliation: Civil and Environmental Engineering Department, Massachusetts Institute of Technology Cambridge, MA, USA.

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.

Show MeSH
Related in: MedlinePlus