REVIEW

published: 07 March 2017

doi: 10.3389/fmicb.2017.00341

Beneficial Microorganisms for Corals

(BMC): Proposed Mechanisms for
Coral Health and Resilience
Raquel S. Peixoto 1,2*, Phillipe M. Rosado 1,2 , Deborah Catharine de Assis Leite 1 ,
Alexandre S. Rosado 1,2 and David G. Bourne 3,4
1
Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil, 2 Instituto Museu
Aquário Marinho do Rio de Janeiro-AquaRio (IMAM/AquaRio) – Rio de Janeiro Marine Aquarium Research Center, Rio de
Janeiro, Brazil, 3 College of Science and Engineering, James Cook University, Townsville, QLD, Australia, 4 Australian Institute
of Marine Science, Townsville, QLD, Australia

The symbiotic association between the coral animal and its endosymbiotic dinoflagellate
partner Symbiodinium is central to the success of corals. However, an array of other
microorganisms associated with coral (i.e., Bacteria, Archaea, Fungi, and viruses)
have a complex and intricate role in maintaining homeostasis between corals and
Symbiodinium. Corals are sensitive to shifts in the surrounding environmental conditions.
One of the most widely reported responses of coral to stressful environmental conditions
is bleaching. During this event, corals expel Symbiodinium cells from their gastrodermal
tissues upon experiencing extended seawater temperatures above their thermal
Edited by: threshold. An array of other environmental stressors can also destabilize the coral
Alison Buchan,
University of Tennessee, USA microbiome, resulting in compromised health of the host, which may include disease
Reviewed by: and mortality in the worst scenario. However, the exact mechanisms by which the coral
Michael Sweet, microbiome supports coral health and increases resilience are poorly understood. Earlier
University of Derby, UK
studies of coral microbiology proposed a coral probiotic hypothesis, wherein a dynamic
Erinn Muller,
Mote Marine Laboratory, USA relationship exists between corals and their symbiotic microorganisms, selecting for
*Correspondence: the coral holobiont that is best suited for the prevailing environmental conditions.
Raquel S. Peixoto Here, we discuss the microbial-host relationships within the coral holobiont, along with
[email protected]
their potential roles in maintaining coral health. We propose the term BMC (Beneficial
Specialty section: Microorganisms for Corals) to define (specific) symbionts that promote coral health. This
This article was submitted to term and concept are analogous to the term Plant Growth Promoting Rhizosphere
Aquatic Microbiology,
a section of the journal (PGPR), which has been widely explored and manipulated in the agricultural industry
Frontiers in Microbiology for microorganisms that inhabit the rhizosphere and directly or indirectly promote plant
Received: 17 October 2016 growth and development through the production of regulatory signals, antibiotics and
Accepted: 17 February 2017
Published: 07 March 2017
nutrients. Additionally, we propose and discuss the potential mechanisms of the effects
Citation:
of BMC on corals, suggesting strategies for the use of this knowledge to manipulate
Peixoto RS, Rosado PM, Leite DCA, the microbiome, reversing dysbiosis to restore and protect coral reefs. This may include
Rosado AS and Bourne DG (2017) developing and using BMC consortia as environmental “probiotics” to improve coral
Beneficial Microorganisms for Corals
(BMC): Proposed Mechanisms resistance after bleaching events and/or the use of BMC with other strategies such as
for Coral Health and Resilience. human-assisted acclimation/adaption to shifting environmental conditions.
Front. Microbiol. 8:341.
doi: 10.3389/fmicb.2017.00341 Keywords: beneficial microorganisms for corals, BMC, probiotics, symbiosis, reversing dysbiosis

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Peixoto et al. Beneficial Microorganisms for Corals (BMC)

INTRODUCTION identification, mechanisms of interaction with their host and

their possible manipulation to improve coral fitness. We propose
Microorganisms are key components of all multi-cellular life the term “Beneficial Microorganisms for Corals” (BMC) for these
due to their crucial roles in nutrient cycling and metabolism coral “probiotic” microorganisms, in analogy to the Plant Growth
(Ainsworth et al., 2010; Garren and Azam, 2012; Thompson Promoting Rhizobacteria (PGPR) (Kloepper and Schroth, 1978),
et al., 2014). In the past few decades, the important relationship which are well-described symbionts of plants that possess specific
between coral and its microbial symbionts have been documented mechanisms to promote plant growth and development (Podile
(reviewed in Bourne et al., 2016). However, coral-microbiome and Kishore, 2007; Lugtenberg and Kamilova, 2009). This term
interactions are not yet fully understood due to complex directly refers to the symbiont microorganisms that are players
interactions, which include host modulation of the physiology of in the maintenance and protection of the coral physiological
symbiotic cells (Barott et al., 2015) and the influence of symbiotic balance. This comparison can be made if we define the BMC
cells on their host (Sharp and Ritchie, 2012). The responses of mechanisms that promote coral health and use current published
coral-associated microbial communities to shifts in coral health examples that detail the mechanisms by which candidate BMC
(Harvell et al., 2007; Bourne et al., 2008; Jones et al., 2008; promotes coral health. The network of beneficial interactions
Glasl et al., 2016; Guest et al., 2016) and environmental stressors provided by some symbiotic microorganisms is summarized in
(Hughes et al., 2003; Doney et al., 2012; Vega Thurber et al., Figure 1 and detailed further in subsequent discussion sections.
2014; Garren et al., 2015; Kwiatkowski et al., 2015) have been Within plant sciences, a similar approach has been widely
extensively explored and reported. Changes in environmental explored within the complex rhizo-microbiome environment,
conditions may modify coral physiology, leading to changes which is inhabited by a wide range of microorganisms. Some
in the structure, spatial arrangement and abundance of the beneficial microbes in the rhizosphere improve plant health
local population. These environmental disturbances can also and promote growth through direct and/or indirect mechanisms
directly or indirectly induce shifts in the associated microbial such as enhancement of plant nutrition (e.g., nitrogen fixation,
communities, leading to the emergence of disease (Harvell et al., solubilization of phosphate or production of siderophores),
2007; Mouchka et al., 2010), which is an ongoing threat to coral biological control of plant pathogens and induction of plant
reefs worldwide (Mumby and Steneck, 2008; Harvell et al., 2007; defense systems, among others (Götz et al., 2006; Couillerot et al.,
Vega Thurber et al., 2009; Krediet et al., 2013; Rogers and Miller, 2009; do Carmo et al., 2011; Scheuring and Yu, 2012; Mendes
2013). et al., 2013; Vacheron et al., 2013). We propose to evaluate
Through shuffling of the dominant photosynthetic BMC in the same way, assembling the beneficial mechanisms of
Symbiodinium clades within their tissues, some corals have individual microorganisms to generate a cluster of targets and
become more tolerant to seawater temperature increases, thereby search for microbial groups that should be better understood and
avoiding repeated bleaching events (Buddemeier and Fautin, perhaps manipulated to improve coral resilience (see Figure 2).
1993; Baker et al., 2004; Berkelmans and van Oppen, 2006; The selection and application of potential BMC can be achieved
Abrego et al., 2008; Jones et al., 2008). However, corals may by (i), isolating microbial organisms that have potential BMC
revert to the original clade (i.e., sensitive clade) over the long- roles; and (ii), assembling and testing the ability of these BMC
term when the stress is removed (Thornhill et al., 2006). The to convey resilience to corals subject to environmental stress and
coral bacterial communities are also sensitive to environmental biotic and abiotic challenges (both experimentally and in situ).
changes and may also be involved in coral resilience (Reshef et al., Since the coral microbiome is potentially a key factor affecting
2006; Santos et al., 2014, 2015, 2016; Thompson et al., 2014). coral resilience, its manipulation is one action that can be
However, little is understood about the permanence of these shifts developed to protect and preserve coral reefs.
in the coral microbiome in the face of changing environmental
conditions (Rowan et al., 1997; Thornhill et al., 2006; Thompson
et al., 2014) and whether shifting microbial baselines can provide APPLYING THE PROBIOTIC CONCEPT
the resilience needed for corals facing mounting environmental TO CORALS
stresses. Additionally, some reports have also indicated the
importance of the coral genome to resilience (Barshis et al., 2013; Discussion of the term “probiotic” is important to evaluate
Bhattacharya et al., 2016; Howells et al., 2016). Thus, there is still and determine its applicability to BMC. While there are several
much to be explored about the relationship and the actual role definitions of the term “probiotic,” it is widely used in the
of coral-associated microbiota—including Symbiodinium—in context of “a live microbial feed supplement that beneficially
healthy conditions or when homeostasis breaks down. affects the host animal by improving its intestinal balance”
The “Coral Probiotic Hypothesis” (CPH) (Reshef et al., (Fuller, 1989). It was first created to refer to gram-positive
2006) postulates that the coral microbiome can be modulated bacteria associated with the genus Lactobacillus and its effects
to improve coral health and resilience. Little is currently in mammalian hosts (Fuller, 1989; Verschuere et al., 2000). The
known about the mechanisms related to the “probiotic” definition provided by the Food and Agriculture Organization
protection provided by the coral microbiome and whether of the United Nations and the World Health Organization
these mechanisms can actually be considered “probiotics”. (FAO/WHO, 2001/2002) is “live microorganisms that, when
The objective of this review is to focus on the role of administered in adequate amounts, confer a health benefit to the
beneficial microorganisms associated with coral, including their host.” When proposing the CPH, Reshef et al. (2006) asserted

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Peixoto et al. Beneficial Microorganisms for Corals (BMC)

FIGURE 1 | Possible roles and relationships between corals and their symbionts and symbiotic microbial groups. It is important to highlight that these
mechanisms and interactions are some examples of potential BMC mechanisms. Other BMC roles still to be discovered are likely to be important targets in future
investigations.

that the term “probiotic” could also be applied to invertebrates adaptation of the terminology, and considering the international
such as corals. Although corals and other marine invertebrates requirements for classifying probiotic products (Hill et al., 2014),
do not themselves possess an intestine, they harbor diverse we herein propose the use of the term BMC to specifically
microorganisms that assist in the maintenance of their fitness address coral symbionts that possess potential beneficial traits,
(Krediet et al., 2013; Thompson et al., 2014). The use of the term including nutritional (“probiotics”) and protective mechanisms
“probiotic” to simply describe microorganisms that can provide that improve coral fitness and contribute to coral resilience (see
benefits to the host (pro – “in favor of something” and “biotic” – Table 1 and Figure 1).
biological) or their ecosystems would be a natural adaptation of
this term. However, we must also consider that the most accurate
meaning of the term “probiotic” is restricted and encompasses BMC MECHANISMS
features that are needed to determine probiotic assignment. The
International Scientific Association for Probiotics and Prebiotics The coral holobiont comprises the coral host and its associated
(ISAPP) recognizes an overall framework for the use of the term microorganisms, including Symbiodinium, bacteria, viruses,
“probiotic” (Hill et al., 2014) and discusses the regulation of archaea, fungi, endolithic algae and protists (Rohwer et al.,
these products, which is not trivial. Furthermore, coral symbionts 2002; Rosenberg et al., 2007). Distinct microbial communities
can provide many advantages to corals other than nutritional can colonize various coral microhabitats, such as the surface
benefits, including biological control of pathogens. PGPR provide mucopolysaccharide layer (SML), coral tissue, gastrovascular
similar beneficial features in plants (Kloepper and Schroth, 1978), cavity and coral skeleton (Rosenberg et al., 2007; Agostini et al.,
which are widely used to improve agricultural sustainability and 2012; Glasl et al., 2016). A number of other organisms, including
productivity (Peixoto et al., 2010; Singh et al., 2011; Bhardwaj fishes, crabs, and a range of crustaceans, bivalves and worms also
et al., 2014). The CPH is an important and acceptable explanation belong to the group of eukaryotes associated with coral tissue
of the intrinsic relationship within the holobiont. Although and its calcareous skeleton (Rosenberg et al., 2007; Bourne et al.,
the use of the term “probiotic” is not wrong as a natural 2009; Ainsworth et al., 2010; Janouškovec et al., 2013; Šlapeta and

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Peixoto et al. Beneficial Microorganisms for Corals (BMC)

FIGURE 2 | Potential strategies for identifying and application of Beneficial Microorganisms for Corals (BMCs) for increasing coral resilience. The first
step would be to randomly isolate microorganisms from the surrounding reef water and the target coral species. Then the BMC would be identified and screened for
beneficial interactions with the coral host through aquarium based experiments and the mechanisms by which the microorganisms confers benefits to the coral host
identified. Extensive screening of BMCs would be undertaken to ensure no pathogenic interactions occurs and investigate potential antagonistic interactions
between consortia of selected BMCs. The final steps would be application of the developed strategy in large mesocosm systems under relevant environmental
stress conditions and including bacterial challenges to assess effectiveness of treatments before any field trials can begin.

Linares, 2013). Although the diversity of organisms that interact the production of protective molecules such as mycosporine-
with the coral host is highly dynamic and often poorly described, like amino acids (MAA) (Dunlap and Shick, 1998) and can
the wide variety in the coral-associated microbiome enhances the enhance the survival of skeletogenic cell types (Domart-Coulon
range of potential BMC functions that these microorganisms can et al., 2004) (Figure 1). Table 1 identifies some of the most
play in the holobiont. promising candidate BMCs and their interactions within the
The coral holobiont concept provides a framework to discuss coral holobiont, which can potentially be modulated to facilitate
how the associations among the different groups and shifts in improved coral fitness and resilience to environmental shifts.
these associations can influence coral health and the holobiont
symbiotic community (Bourne et al., 2016). Coral-associated Carbon Cycling
microorganisms have important roles in maintaining dynamic Photosynthesis, the process of producing fixed carbon from
holobiont homeostasis, forming a network of connections carbon dioxide and water using light-derived energy, is one
that include carbon uptake, nitrogen and sulfur cycling and of the most important known BMC mechanisms provided by
production of antimicrobial agents, thereby facilitating biological the endosymbiotic Symbiodinium present within the cnidarian’s
control of pathogens (Ainsworth et al., 2010; Krediet et al., gastrodermis cells (Wakefield et al., 2000) (Table 1 and Figure 1).
2013; Raina et al., 2016) (Table 1 and Figure 1). In addition, Symbiodinium are highly efficient in their use of solar energy
bacterial biofilms on reef substrata can serve as cues to facilitate (Brodersen et al., 2014), producing organic compounds that
settlement of coral larvae (Hadfield, 2011). Coral-associated fungi contribute significantly to coral nutrition. Approximately 60–
can also protect coral tissue against ultraviolet radiation through 80% of Symbiodinium photosynthetic fixed carbon is transferred

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Peixoto et al. Beneficial Microorganisms for Corals (BMC)

TABLE 1 | Examples of proposed BMC (beneficial microorganisms for corals) characteristics and potential beneficial mechanisms.

Proposed Beneficial Characteristic Beneficial mechanism Examples of references describing the beneficial
(BMC characteristics) mechanism

Photosynthesis Input of organic compounds to the holobiont Verbruggen and Tribollet, 2011; Burriesci et al., 2012; Davy
et al., 2012; Tremblay et al., 2012
Nitrogen fixation Input of fixed nitrogen to the holobiont Olson et al., 2009; Lema et al., 2012; Santos et al., 2014;
Bednarz et al., 2015; Cardini et al., 2015
Fixed nitrogen and carbon cycling and Control of organic compound distribution Kimes et al., 2010
regulation
Production of Bacterial populations control on the coral Barott and Rohwer, 2012
dimethylsulfoniopropionate (DMSP) surface
Degradation of Increase carbon and sulfur availability; Kirkwood et al., 2010; Raina et al., 2016
dimethylsulfoniopropionate (DMSP) production of sulfur-based antimicrobial
compounds such as tropodithietic acid (TDA)
Production of mediated signals to larval Contribute to larval settlement modulation or Webster et al., 2004; Heyward and Negri, 2010;
settlement facilitation regulation Ritson-Williams et al., 2010; Shikuma et al., 2014
Production of antibiotics and Biological control of pathogens Ritchie, 2006; Gochfeld and Aeby, 2008; Kirkwood et al.,
competition with pathogens 2010; Alagely et al., 2011; Kvennefors et al., 2012
Production of quorum sensing (QS) Allow microbial interactions within the Henke and Bassler, 2004; Ng and Bassler, 2009; Tait et al.,
signal molecules, such as holobiont; can act on bacterial colonization 2010; Sharp and Ritchie, 2012; Certner and Vollmer, 2015;
N-acylhomoserine lactones (AHLs) control, bioluminescence, pathogenesis control Meyer et al., 2015
and extracellular enzyme production
Mechanisms influencing the protection Enhance the survival of skeletogenic cell types Domart-Coulon et al., 2004
of skeletogenic cells
Production of mycosporine-like amino Protection of coral tissue against ultraviolet Dunlap and Shick, 1998
acids (MAA) radiation

to the coral host (Tremblay et al., 2012), primarily as glucose Manipulation of Symbiodinium populations in hospite, i.e.,
(Burriesci et al., 2012). This glucose is used for coral growth, inoculating more thermally tolerant strains (as part of BMC
reproduction, respiration and biocalcification (Davy et al., 2012). consortia, as described in Figure 2), is one mechanism to
A variety of Symbiodinium strains have been identified and are increase the resilience of the coral holobiont to thermal stress
distributed into 9 clades (A–I) (Pochon et al., 2006; Pochon and (Berkelmans and van Oppen, 2006; van Oppen et al., 2015).
Gates, 2010; Blackall et al., 2015). However, only 6 have been Symbiodinium are often manipulated in nature itself; corals can
identified in corals: A, B, C (Rowan and Powers, 1991), D (Baker, naturally shuffle Symbiodinium populations with some being
2003), F (LaJeunesse, 2001) and G (Van Oppen et al., 2005). Type more heat tolerant (Buddemeier and Fautin, 1993; Baker et al.,
D symbionts are known to be the most heat tolerant (Silverstein 2004, 2016; Berkelmans and van Oppen, 2006; Abrego et al.,
et al., 2017), and as such, corals subject to repeated bleaching 2008; Jones et al., 2008). However, the long-term stability of
events have a higher proportion of this symbiont (Baker et al., manipulated coral/Symbiodinium associations is still unclear and
2004; Berkelmans and van Oppen, 2006; Stat and Gates, 2011; requires further investigation (Thornhill et al., 2006; Baker et al.,
Lesser et al., 2013; Silverstein et al., 2017). Recent data from 2016). Efforts centered on coral propagation and reef restoration
a rare Symbiodinium biosphere have demonstrated the de novo are increasing globally (Young et al., 2012), in response to
acquisition of Symbiodinium types from surrounding water by alarming declines in coral reefs in some regions of the world
adult corals and indicate that an important switching strategy (Hoegh-Guldberg et al., 2008; De’ath et al., 2012). These efforts
may contribute to holobiont thermal tolerance (Boulotte et al., offer the opportunity to test the manipulation of Symbiodinium
2016). It is known that corals in some of the hottest seas of the strains through inoculation of early life stages of corals with
world have developed a symbiotic relationship with algae, which resilient clades that offer the best hope for growth and survival
facilitates thermal tolerance to the host (Howells et al., 2013; in restoration areas. However, the trade-offs in coral life history
Hume et al., 2015). The genomic blue-print of Symbiodinium traits must be fully explored to ensure that such manipulations
is beginning to be unveiled; comparative analyses demonstrate do not solve one problem and introduce another into the coral
that all dinoflagellates have significantly more transmembrane population.
transporters, especially those associated with carbon and nitrogen Many current studies are focused on identifying the
delivery, compared to other eukaryotes (Aranda et al., 2016). prokaryotes associated with corals and, more importantly,
Species-specific expansions in these transporters can potentially elucidating their function, including pathways for nutrient
provide a genomic explanation for specific Symbiodinium clade sharing and passage within the holobiont (reviewed in Bourne
adaptations to different hosts and environments. Increasing et al., 2016). This ability of microbes to metabolize nutrients,
genomic information for all BMCs, including Symbiodinium, will which can then be translocated to their host, is likely
help to identify traits essential for symbiosis and the shared a driver in the establishment of coral-associated microbial
functional capacity that is critical for a stable coral holobiont. assemblages. Coral metagenomic studies are beginning to identify

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Peixoto et al. Beneficial Microorganisms for Corals (BMC)

several genes in the central carbon metabolism pathways, (Olson et al., 2009; Lema et al., 2012; Santos et al., 2014). The
including carbon fixation and degradation genes (Kimes et al., nitrogen provided by this process is likely to support the host
2010). However, the presence of a functional gene does not and its associated microbiota, including Symbiodinium (Santos
necessarily imply functionality, and further in situ research or et al., 2014). It is estimated that diazotrophs provide up to
metatranscriptomic and metabolomic analyses are needed to 11% of Symbiodinium nitrogen requirements (Cardini et al.,
improve our knowledge of the role of the microorganisms in 2015). Lesser et al. (2007) demonstrated that Symbiodinium
driving nutrient cycling in corals. cells associated with Montastrea cavernosa acquire N from
Williams et al. (2015) have suggested a potential, and cyanobacterial endosymbiotic diazotrophs; this ability seems
important, role of the endolithic algae influencing the to increase with depth and is dependent on heterotrophy. In
bacterial diversity within the coral tissue. Endolithic microbial addition, some fungal species have been hypothesized to be
communities are often a forgotten component of the coral involved in nitrogen metabolism through conversion of nitrate
holobiont (Yang et al., 2016). These organisms have also a and nitrite to ammonia, thereby enabling fixed nitrogen to cycle
potential active role in protecting corals during bleaching events within the coral holobiont (Wegley et al., 2007). Archaea may
through basal photosynthetic activity, translocating nutrients also be central to nitrogen recycling within corals, likely through
from the skeleton to the coral tissue and keeping the coral alive nitrification and denitrification processes, and thus regulate
until re-colonization of Symbiodinium (Fine and Loya, 2002; ammonium concentrations (Siboni et al., 2012).
Verbruggen and Tribollet, 2011). A greater understanding of the Members of the Roseobacteriales group (also involved
function of all prokaryote communities and their niche location in sulfur cycling) are often identified as obligate associates
within the holobiont is essential to defining the BMC and then within Symbiodinium cultures, increasing the growth rate of
elucidating mechanisms to manipulate them for the benefit dinoflagellates (Ritchie, 2011). Bacteria/algae interactions can be
of corals. For instance, the use of network analysis, evaluating affected under environmental disturbance and, in turn, can affect
negative and positive interactions between microorganisms and the holobiont as a whole. Exploring and understanding these
their roles, has been suggested as moving the field of microbial interactions will facilitate the development of methodologies to
ecology in corals forward (Sweet and Bulling, 2017) and would manipulate the nitrogen-fixing microbiome, stimulating specific
be extremely useful to elucidate such mechanisms. groups by adding nutrients or inoculating key BMC groups (BMC
Within the coral holobiont, symbiosis can occur not only consortia) to increase or regulate nitrogen inputs (Figure 2).
between the coral host and its photosymbionts or between Symbiodinium and several bacterial groups have a central
the coral host and its microbiome but also as a mutualistic BMC role within the sulfur cycling pathways of the coral
relationship between the photosymbionts and the microbiome. holobiont (Table 1 and Figure 1). The Symbiodinium are
The growth and density of dinoflagellate populations within large producers of dimethyl sulfate compounds (DSCs), which
the coral host are highly dependent on available nutrients. take part in the antioxidant system of corals (Deschaseaux
As such, the microorganisms mediating nutrient cycling likely et al., 2014) and also potentially in structuring coral-associated
have an important role in the stability of the Symbiodinium bacterial communities that cycle carbon and sulfur within the
population and consequently aid in the maintenance of coral- holobiont (Raina et al., 2009, 2010). Coral-associated bacterial
symbiotic algae interactions (Santos et al., 2014; Rädecker groups, including members of the Flavobacteriaceae (Howard
et al., 2015). This indicates that BMC mechanisms are not et al., 2011) Halomonas (Todd et al., 2010), Roseobacter,
only specific to the coral host but could also be represented Pseudomonas, and Oceanospirillales (Raina et al., 2010, 2013),
by beneficial interactions between coral microbial symbionts. are capable of metabolizing dimethylsulfoniopropionate (DMSP)
Any manipulation must account for these complementary and consuming its products for their own metabolic processes.
interactions within the holobiont. Therefore, the use of consortia The catabolism of DMSP also potentially generates sulfur-based
(as opposed to single-strain inoculation) with a range of antimicrobial compounds such as tropodithietic acid (TDA),
mechanisms for beneficial outcomes for the coral is strongly which at low concentrations (0.5 µg/mL) can inhibit the growth
recommended. However, evaluating the potential benefits and/or of the coral pathogens Vibrio coralliilyticus and V. owensii (Raina
detrimental roles that each BMC has in a consortium, rather than et al., 2016). Thus, the production and metabolism of sulfur
individually, is challenging and requires detailed investigation in compounds represents a potential BMC mechanism, and the
model systems. manipulation of these key microbial groups may promote coral
health through the regulation of key symbiotic populations,
antimicrobial activity and nutrient input.
Other Essential Nutrient Cycling
Pathways
Metagenomic studies have identified the presence of genes Production of Antibiotics and
involved in nitrogen cycling pathways via nitrogen fixation, Competition With Pathogens
ammonification, nitrification, and denitrification within the Recent studies have focused on the biological control promoted
coral holobiont (Wegley et al., 2007). Ubiquitous nitrogen- by native bacteria in the regulation of bacterial colonization
fixing bacteria have been reported in corals as inferred by on the coral surface, which consequently controls resistance
recovery of nitrogenase (nifH) gene diversity, with dominant against diseases (Bourne et al., 2016; Egan and Gardiner,
taxa representing the α-, β-, γ-, and δ-proteobacterial classes 2016; Glasl et al., 2016). Corals can protect themselves against

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pathogen infection using the mucus microbiome as a barrier Choi et al., 2010; Jensen et al., 2010; Yang et al., 2010; Speck
against potential pathogens (Glasl et al., 2016). Some protective and Donachie, 2012; Pike et al., 2013). Additionally, some
mechanisms include competition for nutrients and/or space, Endozoicomonas strains have been identified as producers of
and/or production of antibiotics in mucus (Ritchie, 2006) or antimicrobial compounds (Ritchie, 2006; Rua et al., 2014) and
coral tissue (Gochfeld and Aeby, 2008). Shifts in the native may have a role in sulfur cycling (Raina et al., 2009). Ainsworth
microbial community may have a negative impact on the host, et al. (2015) detected members of the order Endozoicimonaceae
i.e., dysbiosis (Petersen and Round, 2014), leading to the onset in the coral mucus and/or skeleton, though this group was not
of disease and eventual mortality (Egan and Gardiner, 2016). part of the symbiotic core microbiome associated with the coral
For instance, thermal stress can induce changes in coral mucus species Montipora capitate, Acropora granulosa, and Leptoseris
and a consequent shift in the microbiome, which in turn could spp. Altogether, these findings highlight the potential role of
influence holobiont homeostasis (Lee et al., 2016). this group in the biological control of coral pathogens. Recent
Several studies have demonstrated that bacteria isolated genomic studies indicate that Endozoicomonas may be able to
from corals are able to inhibit the colonization and growth recognize, translocate, communicate and modulate the coral
of many other types of bacteria through antibacterial activity, host (Ding et al., 2016) plus contribute to protein provision and
including putative pathogens of coral such as Vibrio shiloi cycling of carbohydrates (Neave et al., 2017). Neave et al. (2017)
(Rypien et al., 2010), V. coralliilyticus (Kvennefors et al., 2012) demonstrated evidence for specific symbiotic mechanisms for
and Serratia marcescens (Alagely et al., 2011). Thus, production different Endozoicomonas ecotypes associated with different
of antibiotics and niche competition with pathogens are strong coral hosts though these ecotypes likely have a non-symbiotic life
BMC mechanisms provided by the coral microbiome (Table 1). stage due to possession of large genomes which have not been
The biological control of bacteria, including pathogens, can also narrowed for obligate endosymbiosis. These studies highlight the
be performed by viruses and protists (Figure 1), which are importance of Endozoicomonas for corals and other marine hosts
the two dominant top–down control mechanisms of bacteria in potentially developing one or more BMC mechanisms.
in the open ocean (Chow et al., 2014). Recent studies have
indicated the important role of viruses in coral fitness, either Quorum Sensing
causing diseases or promoting coral health (reviewed in Sweet Little is known about quorum sensing (QS), a system of
and Bythell, 2016 and Vega-Thurber et al., 2017). Corals can bacterial cell-cell chemical signaling, within the coral holobiont.
harbor a great diversity of bacteriophages and archaeal phages, It is necessary to confirm the production of QS signals by
feasibly involved in key ecological interactions and genetic coral-associated commensals and pathogens under laboratory
material exchange (Sweet and Bythell, 2016), playing a crucial conditions as well as to detect them in natural environments.
role in the reef microbial dynamics and biogeochemical cycling However, evidence from other microbial-host interactions
(Vega-Thurber et al., 2017). However, despite their role in indicates that QS can be a beneficial mechanism to improve
the biological control of specific bacteria, Chow et al. (2014) coral health and resilience through the control of native
correlated shifts in microbial structures and detected positive and/or pathogenic populations. For example, QS systems are
interactions between bacteria and viruses, suggesting that viruses important for PGPRs, specifically legume-nodulating rhizobial
may not only control but also follow their host. This may indicate nitrogen-fixing symbiotic cells, which are strongly influenced
that viruses can control pathogens and be used in association with by QS signaling and often control other bacterial populations
BMC consortia. Successful phage therapy experiments developed (Wisniewski-Dyé and Downie, 2002; Chin-A-Woeng et al., 2003;
in small aquarium demonstrate the prevention of the progression Gonzalez and Marketon, 2003; McAnulla et al., 2007; Sanchez-
of bacterially mediated lesions on infected corals (Efrony et al., Contreras et al., 2007). QS genes are also involved in several
2009; Cohen et al., 2013). Therefore, the effects of viruses on bacterial physiological adaptations (e.g., light and antibiotic
bacterial development and competitiveness should be analyzed production), allowing bacteria to change their behavior and
as a potential factor to be manipulated for enhancing BMC improve niche competitiveness (reviewed in Sanchez-Contreras
effectiveness. et al., 2007).
Some bacterial groups, such as Endozoicomonas, are Quorum sensing may be one mechanism used to modulated
predominant in healthy corals, but the relative abundance bacterial–host interactions at the coral surface (Sharp and Ritchie,
of this group decreases in compromised or diseased corals 2012). Coral mucus/microorganism interactions are likely
(Bayer et al., 2013; Vezzulli et al., 2013; Meyer et al., 2014; competitive, with dominant communities potentially secreting
Glasl et al., 2016; Neave et al., 2016; Morrow et al., 2017). The QS disruptive compounds that influence the colonization,
genus Endozoicomonas belongs to the family Hahellaceae and bioluminescence, pathogenesis and extracellular enzyme
the order Oceanospirillales, a group of heterotrophic aerobic production in a number of bacterial species, including some
marine bacteria that were first described by Kurahashi and from the genus Vibrio (Ng and Bassler, 2009). For example,
Yokota (2007). Although the functional role of Endozoicomonas Vibrio growth dynamics and competitiveness in coral mucus
is not well understood, this genus has been described as a and tissues has been demonstrated to be linked to QS signaling
very diverse and flexible symbiotic group (Neave et al., 2017) molecules such as N-acylhomoserine lactones (AHLs) (Henke
that is associated with several marine hosts and is globally and Bassler, 2004; Tait et al., 2010; Certner and Vollmer, 2015).
distributed. The genus occurs in sponges, fishes, corals and These Vibrio-derived QS molecules are also influenced by
others (Kurahashi and Yokota, 2007; Bourne et al., 2008; environmental factors such as temperature (Tait et al., 2010; Saha

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Peixoto et al. Beneficial Microorganisms for Corals (BMC)

et al., 2015) with QS mechanisms breaking down under stress (2016) detected a stable bacterial community (bacteriome core)
conditions that disrupt the associated microbiome. Certner and associated with six coral species from the Caribbean region,
Vollmer (2015) demonstrated that resident microorganisms suggesting that the host is the stronger driver of this core and
can opportunistically cause white band disease in Acropora also indicating specific and divergent niches for bacteria. While
cervicornis and that this seems to be regulated by a quorum- there is an identifiable core coral microbiome, there is also a
sensing signaling molecule. Manipulating QS mechanisms to dynamic microbiome that varies depending on species, season,
promote beneficial microbes over opportunistic or pathogenic habitat and life stage and is likely a product of stochastic events
microbes is one potential strategy to improve coral fitness during or a response to changing environmental conditions (Hester
times of stress (Table 1). However, it is necessary to increase et al., 2015). This dynamic community is also an important target
our knowledge of these interactions to establish a successful for BMC studies because it can represent a source of strains
manipulation process. that are adaptive to specific conditions of environmental stress.
Acquisition and/or shifts in microorganisms have been suggested
as an important tool for coral adaptation and are potentially one
CORE MICROBIOME: A USEFUL CORAL mechanism for increasing resilience under varied environmental
HEALTH INDICATOR conditions (Zilber-Rosenberg and Rosenberg, 2008; Singh et al.,
2013; Ziegler et al., 2017).
Defining the stable and ubiquitous core microbiome, the variable Beneficial Microorganisms for Corals should be identified and
microbial species associated with coral (and responsive to potentially manipulated for each individual coral species, each
environmental conditions) and the spatially and/or regionally regional location and each stage of development. For example,
microbial core (niche-specific) (Hernandez-Agreda et al., 2016; in the case of humans, a doctor will always provide individual
Sweet and Bulling, 2017) can inform the health status of coral analysis, considering specific medical records pertaining to a
relative to the environment and constitutes a viable approach specific patient, including their age, prior to prescribing a
to identify potential BMCs. The core microbiome is composed medication or treatment. Likewise, a microbial consortium,
of common members, host-specific, of two or more microbial specifically isolated from and developed for oil bioremediation
communities (Turnbaugh et al., 2007; Hamady and Knight, 2009; in polar areas, may not be the best option for oil bioremediation
Hernandez-Agreda et al., 2016; Sweet and Bulling, 2017). Studies in tropical areas because strains may not be well adapted
have suggested that identification of the operational taxonomic to a new environment with a range of different biotic and
units (OTUs) that compose the core microbiome is vital because abiotic interactions. Environmental recovery and protection
these populations may play key roles (potential BMC) due to strategies can be applied to various habitats, provided that
their ability to maintain stability in the face of environmental they are subject to the local conditions of that environment.
changes (Shade and Handelsman, 2012; Shafquat et al., 2014; It is important to follow strict ethical guidelines, as currently
Ainsworth et al., 2015; Chu and Vollmer, 2016). This approach indicated for microbiome studies and manipulation of other
has been applied to identify the interactions between other organisms (Rhodes et al., 2013), to avoid undesirable side effects.
hosts and microorganisms, including mammalian intestines and The manipulation of native and non-modified microorganisms is
plant roots (Shade and Handelsman, 2012; Shafquat et al., the first step to achieve this.
2014). Identification of the central metabolic pathways associated
with the core microbiome will also provide vital information
about how host–microbiome interactions are established and Coral Diseases, A Disruption Within The
maintained (Shafquat et al., 2014; Ainsworth et al., 2015). The Bmcs?
“functional coral core microbiome” is potentially more important Coral diseases may occur in response to biotic stresses caused
than a taxonomic core, as demonstrated for seaweeds, with by bacteria, fungi, and viruses (Davy et al., 2006; Bourne et al.,
functional redundancy widely observed in complex microbial 2009; Krediet et al., 2013) and/or abiotic stresses, such as rising
communities (Burke et al., 2011). Therefore, while microbial temperature, ultraviolet radiation, sedimentation and pollution
community diversity may change in response to environmental (Harvell et al., 2002, 2007; Bruno et al., 2003; Burge et al., 2014).
conditions, essential functions can be maintained by the The disruption of the BMC community (both core and dynamic
new taxonomic groups. Importantly, the core microbiome is microbial communities) is likely an important trigger for disease
commonly associated with host-constructed niches, and these establishment. The term “disease” has a variety of definitions
microorganisms are therefore less sensitive to the surrounding and essentially describes a shift away from a healthy state that
environment (Hester et al., 2015). However, they are also may be caused by exogenous (external, environmental) and
potentially capable of adapting to environmental change (McFall- endogenous (internal, from the organism itself) factors (Scully,
Ngai et al., 2013; Santos et al., 2014). 2004). In recent years, coral diseases have emerged as a significant
Ainsworth et al. (2015) identified the bacterial symbionts that threat to reefs around the world. From the time the first coral
compose the core microbiome in the corals Acropora granulosa, disease was described in Antonius (1973) to today, more than
Montipora capitata, and Leptoseris spp. The core microbiome 30 diseases have been reported (Green and Bruckner, 2000),
in various coral niches were identified, including bacteria which demands an urgency in understanding coral–microbiome
specific to the gastrodermis cells and symbiotic Symbiodinium interactions. In general, these diseases are identified by changes
dinoflagellates (Ainsworth et al., 2015). Chu and Vollmer in coral coloration, whose characteristics provide the names of

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Peixoto et al. Beneficial Microorganisms for Corals (BMC)

the diseases, such as black band, white band, yellow band, and thereby transfer a BMC cocktail directly into the coelenteron.
white pox, among others. Coral diseases have the potential to Use of knowledge derived from other systems will be essential
cause widespread mortality and thereby significantly change the to develop inoculation strategies suitable for corals. For example,
structure of reef communities (Porter et al., 2001; Sutherland and microbial saline suspension and microbial immobilization of
Ritchie, 2004; Miller et al., 2009). However, little is known about substrates such as biodegradable polymers are currently used in
the causes and effects of these diseases, including the etiology, terrestrial environments (Ahmad et al., 2011) and aquaculture
transmission route, prevention, control and reduction of their systems (Martínez Cruz et al., 2012). The use of cost-
impacts. Disruption of homeostasis may result in physiological effectiveness and biodegradable substrates, such as the widely
changes that may cause disease or even lead to the mortality used alginate (Sivakumar et al., 2014), could potentially represent
of the whole colony. It is possible that this disruption is an environmentally friendly approach to encapsulation of BMCs
caused by an imbalance in BMC mechanisms, or dysbiosis, i.e., and delivery to corals as heterotrophic feed particles, essentially
loss of antimicrobials and loss of nutritional pathways, which similar to probiotics in humans.
then leads to disease. The mechanisms of disruption could be Microbiome manipulation to enhance coral health could be
unveiled by BMC studies, where the absence of benefits can used in association with other approaches for better results
be regarded as potential disease mechanisms. For instance, it (Figure 2). For instance, human-assisted evolution (HAE) of
is suggested that Symbiodinium cells require nitrogen that is coral involves the genetic natural enhancement of corals to
provided by coral-associated nitrogen-fixing bacteria (Cardini improve their tolerance to stress (van Oppen et al., 2015). Some
et al., 2015). However, environmental thermal disturbances lead techniques may be used to naturally accelerate coral adaptation
to changes in the abundance and diversity of these nitrogen- against these stresses, such as random mutations, natural
fixing communities (Santos et al., 2014). Initially, the holobiont selection, acclimatization and random changes in microbial
can adapt to supply Symbiodinium and consequently meet symbiont communities (van Oppen et al., 2015). The human-
coral requirements. However, if a thermal disturbance persists, assisted evolution of corals could be developed in association with
it is likely that a breakdown in the homeostasis may occur. the use of specific BMC consortia inoculants for specific coral
Knowledge of BMC mechanisms and symbiotic relationships species and environmental conditions, in addition to inducing
within coral could potentially aid in the development of the modulation of naturally generated microbiota in corals.
microbiome management strategies that may avoid any such BMC could be continually used during various stages of coral
disruption in coral/microbial associations (Figure 2) and reverse development (Figure 2), to thereby increase the coral survival
dysbiosis. For instance, specific nitrogen-fixing bacteria could be rate. The use of phage therapy associated with BMC is also
inoculated during events of thermal stress. This procedure could a promising approach to be tested, as BMC could improve
delay the effects of environmental impact within the holobiont, coral fitness and phage could act to directly control potential
which would then be capable of withstanding environmental pathogens.
stress until the restoration of optimal environmental conditions. The host–microbial interaction data provided by these
It is important to understand the crucial breaking point when the experiments could be used to indicate functional microbiome
symbiotic interaction fails; fine-scale and dynamic observation dynamics at different coral life stages. Induced shifts in the
of both host and symbiont function will be required to do so. microbiome of sensitive or diseased corals through the use of
For instance, the phylogenetic and functional response of sponge BMC consortia inoculants or modulated BMC populations are
holobionts to thermal stress was thoroughly described by Fan plausible options and could be considered an epigenetic process
et al. (2013). Such comprehensive surveys are needed to fully of acclimation (Heard and Martienssen, 2014). Furthermore,
understand what and when imbalances occur and pass a point experiments that breed corals, maintain offspring under future
of no return. climate scenarios (i.e., elevated temperature) and evaluate
native microbiome responses under thermal stress conditions
could provide important information about the contribution
POTENTIAL MANIPULATION OF BMCs of BMC to coral resilience. Inoculation of various types of
Symbiodinium at various temperatures and the analysis of
The recovery and selection of potential BMC could be developed the competitiveness of these different types, as well as the
through basic microbiology methods using tailored culture resilience potential of inoculated corals, would also provide
media and cultivation strategies and screening for specific important BMC mechanistic data that will be the basis of further
mechanisms (Figure 1). The selection of culture media can manipulation. To evaluate the concept of protection transmission
be targeted to our current understanding of the nutritional from resistant to sensitive corals, transplantation of the microbial
requirements of potential BMC organisms. BMC can be community via inoculation of healthy macerated tissue from
inoculated at different coral life stages, such as larval and or disease-resistant corals to sensitive ones (similar to fecal
juvenile stages, prior to acquisition of Symbiodinium using transplant) could also be tested. However, the concentrations
similar approaches to those performed in agriculture through of each of the protective populations may not be sufficiently
the inoculation of seeds with PGPRs (Götz et al., 2006). BMC high to support competitiveness of these beneficial introduced
inoculation could also be performed on adult corals with populations. It would also be interesting to encourage similar
potentially novel applications, such as using microencapsulation approaches extrapolating the term BMC to other marine hosts
and nanoparticles to heterotrophically feed adult corals and [i.e., Beneficial Microorganisms for Sponges (BMS), Beneficial

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Peixoto et al. Beneficial Microorganisms for Corals (BMC)

Microorganisms for Seagrass (BMS), etc.] by manipulating and Cury et al., 2015; Jesus et al., 2015). Even within these
evaluating specific mechanisms related to varied marine hosts well-defined systems, microbiome manipulation is challenging
and evaluating the ecological data regarding marine host– due to the evolving and complex nature of host/microorganism
microbiome interactions. interactions.
The selected and proposed mechanisms can, and should, It is also important to highlight that BMC and the strategies
be also expanded, as more information on the microbial for their application, must be tested in well controlled,
beneficial traits for corals are described. There are several realistic experimental systems before field application. Before
potential mechanisms to be explored to improve coral fitness. initiating reef recovery, it is best to perform a survey of the
For instance, the production of reactive oxygen species (ROS) target reef to determine which components would be more
is a key response of marine organisms against environmental suitable to improve the health of the site. Factors such as
stress, such as thermal stress (Lesser, 2012). In the absence the stability of the host/microbial associated community, the
of a definite mechanism for coral bleaching, the most widely microbiome transmission route (i.e., vertical vs. horizontal)
accepted model is that Symbiodinium sp. chloroplasts are and the cross-species relationships (neutral, beneficial or
heat-damaged by the light-induced generation of toxic ROS, pathogenic) must be established. For instance, it is important
which could also be associated with other cellular processes to ensure that selected BMC microorganisms are not members
and pathways (Tolleter et al., 2013). Although several types of the “Pathobiome”; a term recently suggested by Sweet
of ROS have been described, with a gradient of reactivity and Bulling (2017) identifying the pathogenic members of
and diffusivity across membranes (Lesser, 2006), the primary the microbiome. As highlighted by Sweet and Bulling (2017),
mechanism of ROS production in Symbiodinium seems it is essential to understand the pathobiome members and
to be through hydrogen peroxide formation at the end of the mechanisms of interaction within the holobiont. This
the photosynthetic electron transport chain. Suggett et al. concept is complementary to the BMC concept, as both aim
(2008) suggested that the thermal tolerance of Symbiodinium to better understand the mechanisms of dysbiosis and the
could be associated with adaptive restrictions related to triggers of microbiome disruption within the holobiont. Strict
photosynthesis and correlated sensitive phylotypes with higher and robust testing of BMCs must be performed in small
H2 O2 production. Increasing the in hospite concentration of scale experimental systems and scaled up to mesocosms, which
catalase—an enzyme commonly found in organisms exposed to mimic field conditions, before field application. Questions such
oxygen that catalyzes the decomposition of hydrogen peroxide as in situ microorganism growth characteristics, effectiveness,
to water and oxygen (Chelikani et al., 2004)— within the competitiveness (interactions between host and inoculated
holobiont could minimize the concentration of ROS during BMC), trade-offs, repeatability and mass application (ecosystem
periods of thermal stress. Exploiting the ability of specific scale) all need to be considered and evaluated. Although
coral-associated microorganisms to increase catalase production potentially efficient, microbial manipulation is very specific, and
represents a BMC target to be explored as a potential BMC specific studies and strategies must be applied for each site.
mechanism and mitigation strategy to minimize and buffer
against severe bleaching episodes. Considering that there
are other enzymes that harvest ROS, such as super oxide CONCLUSION AND PERSPECTIVES
dismutase and lysozyme, several other mechanisms can be ABOUT BMC
suggested and evaluated to minimize ROS concentration
within corals under thermal stress, as research focusing Coral microbiologists continue to describe the potential
on coral microbiome manipulation start to be developed. mechanisms by which corals benefit from associations
Likewise, several other groups and mechanisms should be with microbial partners (Table 1), and the application of
better explored as potential BMC, including groups, such “omics”-based approaches will further provide important
as cyanobacteria and endolithic algae. Research focusing information about the BMCs associated with corals. We propose
on coral microbiome manipulation is beginning to be that microorganisms possessing at least one of the listed
developed. characteristics detailed in Table 1 could be classified as a BMC
and manipulated to assess potential effect on coral fitness and
resilience. This approach requires robust assessment of the
CHALLENGES AND CONCERNS efficiency and safety, however, in laboratory conditions before
field application, similar to what is undertaken in agriculture,
Studies of microbiome manipulations have, to date, mostly bioremediation and probiotic use by humans. These approaches
focused on terrestrial hosts (Alivisatos et al., 2015) such as will be challenging and there are many large knowledge gaps that
biological control and PGPR inoculants for agricultural purposes need to be filled before BMCs can be suitable to the real world.
(Costa et al., 2006; Götz et al., 2006; Peixoto et al., 2006, However, the first step is to encourage the discussion around
2010; Aboim et al., 2008; Berg, 2009; Rachid et al., 2013), the concept for corals and its possibilities for reef ecosystems.
human fecal transplants (van Nood et al., 2013) and probiotics The second step is undertaking well designed laboratory based
for humans (Leite et al., 2013, 2015). Bioaugmentation or experimental manipulations of BMCs, evaluating the health
microbiome manipulation approaches are also very useful for outcomes for coral holobionts under different environmental
the bioremediation of contaminated sites (Santos et al., 2011; conditions. Successful examples of microbial modulation in other

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Peixoto et al. Beneficial Microorganisms for Corals (BMC)

organisms can guide these efforts to test BMCs. Considering AUTHOR CONTRIBUTIONS
the alarming declines reported for coral reefs globally (Hoegh-
Guldberg et al., 2008) innovative solutions are required to All authors listed, have made substantial, direct and
halt or even reverse these trends. While manipulation of the intellectual contribution to the work, and approved it for
microbiome to improve coral resilience may be challenging publication.
and even controversial, the necessity to preserve coral reefs is
paramount and all options should be on the table. In fact, a
“natural BMC manipulation” of the bacterial community (i.e., a ACKNOWLEDGMENTS
positive correlation between bacterial community dynamics and
coral heat tolerance), was recently suggested by Ziegler et al. The authors thank Prof. Torsten Thomas (UNSW) for his
(2017). At the very least, application of the BMC concept and critical comments and helpful suggestions to improve the
manipulation of identified BMC candidates can improve our manuscript. The authors would like to thank Conselho
understanding of the vital role microbes play within the coral Nacional de Desenvolvimento Científico e Tecnológico (CNPq),
holobiont through integrative physiological, microbiological and Fundação de Amparo à Pesquisa do Estado do Rio de
‘omic’ based approaches. Such detailed understanding is critical Janeiro (FAPERJ), Coordenação de Aperfeiçoamento de Pessoal
for corals and the reef ecosystems that they build, faced with de Nível Superior (CAPES) and Instituto Museu Aquário
on-going global declines. Coral “microbial-therapy” is a potential Marinho do Rio de Janeiro-AquaRio (IMAM/AquaRio) – Rio
new area of study in the face of increasing threats to coral reefs de Janeiro Marine Aquarium Research Center, Rio de Janeiro,
that could have positive outcomes for reefs in the near future. Brazil.

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Antonie van Leeuwenhoek 81, 397–407. doi: 10.1023/A:1020501104051 conducted in the absence of any commercial or financial relationships that could
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(2010). Endozoicomonas montiporae sp. nov., isolated from the encrusting
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Yang, S.-H., Lee, S. T. M., Huang, C.-R., Tseng, C.-H., Chiang, P.-W., Chen, C.- (CC BY). The use, distribution or reproduction in other forums is permitted, provided
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1078–1086. doi: 10.1002/lno.10277 or reproduction is permitted which does not comply with these terms.

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