Microbial Interactions on Coral Surfaces and Within the Coral Holobiont
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See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/307910113 Microbial Interactions on Coral Surfaces and Within the Coral Holobiont Chapter · January 2016 DOI: 10.1007/978-3-319-31305-4_21 CITATIONS READS 0 9 4 authors: Max Teplitski Cory J Krediet Smithsonian Institution Eckerd College 114 PUBLICATIONS 2,950 CITATIONS 24 PUBLICATIONS 264 CITATIONS SEE PROFILE SEE PROFILE Julie L Meyer Kim B Ritchie University of Florida University of South Carolina Beaufort 33 PUBLICATIONS 602 CITATIONS 63 PUBLICATIONS 3,043 CITATIONS SEE PROFILE SEE PROFILE All in-text references underlined in blue are linked to publications on ResearchGate, Available from: Cory J Krediet letting you access and read them immediately. Retrieved on: 13 September 2016 Microbial Interactions on Coral Surfaces and Within the Coral Holobiont 21 Max Teplitski , Cory J. Krediet , Julie L. Meyer , and Kim B. Ritchie Abstract Microbial communities associated with coral surfaces are diverse and complex. They play key roles in nutrient acquisition by coral holobionts and in responses to stressors and dis- eases. Members of coral-associated microbiota produce antimicrobial compounds, inhibit cell-to-cell signaling, and disrupt virulence in opportunistic pathogens. Characterization of coral-associated microbial communities suggests that metabolic capabilities defi ne the core members of the communities. However, some taxonomic conservation is becoming evident in microbial communities associated with the same coral species and genera in different geographic regions. Even though shifts in the composition of coral microbiota often corre- late with the appearance of signs of diseases and/or bleaching, it is not yet clear to what extent these shifts are a cause or a consequence of diseases. This chapter focuses on interac- tions within coral-associated microbial communities and suggests potentially interesting directions for future research. Keywords Coral microbiology • Coral disease • Halomonas spp. • Coral mucus • Coral commensal microbiota 21.1 Microbial Partners Within the Coral symbiotic entity ; a holobiont (and its hologenome ) is a unit Holobiont: An Overview of evolutionary selection (Rosenberg et al. 2007 ; Rosenberg and Zilber-Rosenberg 2011 ; Rohwer et al. 2002 ). In the case Microorganisms play critical roles in marine, freshwater, and of the coral holobionts, these multi-partite symbiotic organ- terrestrial ecosystems. Recognition of the unique role of the isms are formed by polyp animals, photosynthetic dinofl a- microbiota in eukaryotic host development and response to gellates , and microbial associates of polyps and stressors has led to the concept of a “holobiont,” which is dinofl agellates (Rohwer et al. 2002 ). Dinofl agellates from now used to describe a complex co-evolved multi-partner the genus Symbiodinium are harbored within membrane- bound vacuoles formed inside gastrodermal cells of the Cory J. Krediet and Julie L. Meyer contributed equally to the prepara- tion of this manuscript M. Teplitski (*) J. L. Meyer Smithsonian Marine Station , Soil and Water Science Department , University of Florida , 701 Seaway Dr. , Ft. Pierce , FL 34949 , USA 2033 Mowry Rd , Gainesville , FL 32611 , USA e-mail: maxtep@ufl .edu e-mail: juliemeyer@ufl .edu C. J. Krediet K. B. Ritchie Department of Marine Science , Eckerd College , Mote Marine Laboratory , 1600 Ken Thompson Pkwy , 4200 54th Ave S , St. Petersburg , FL 33711 , USA Sarasota , FL 34236 , USA e-mail: [email protected] e-mail: [email protected] © Springer International Publishing Switzerland 2016 331 S. Goffredo, Z. Dubinsky (eds.), The Cnidaria, Past, Present and Future, DOI 10.1007/978-3-319-31305-4_21 332 M. Teplitski et al. polyp. Dinofl agellates play at least two important roles in the from the environment by the host at very early stages of lar- holobiont. Over half (and up to 90 %) of photosynthate that val development , regardless of the coral reproductive they produce is translocated to the coral host , providing strategy . much of the host’s carbon needs (Tremblay et al. 2012 ; The composition of coral-associated microbial communi- Muscatine et al. 1981 ). Symbiodinium also produces high ties appears to be quite conserved. High throughput sequenc- levels of dimethylsulfoniopropionate ( DMSP ) , which has ing revealed that commensal microbiota of multiple functions in the holobiont: DMSP serves as an Montastraea / Orbicella corals is dominated by the members osmolite and antioxidant for both the alga and the coral of the Halomonas spp. (Meyer et al. 2015 ). Interestingly, (Kirst 1990 ; Deschaseaux et al. 2014 ). It is a nutrient source even when corals were removed from their natural ecosys- for coral-associated bacteria , although the ability to utilize tem and were maintained in an aquarium for over a year, DMSP is broadly distributed in marine microbes (Cui et al. their microbiota were only modestly changed. As shown in 2015 ). DMSP is an important chemical cue for a number of Fig. 21.1 , Halomonas and Moritella spp. were most abun- different organisms, from coral pathogens to reef fi shes and dant members of the communities of corals sampled in the penguins (Garren et al. 2014 ; DeBose et al. 2008 ; Nevitt wild and then maintained in aquaria, even though an expan- 2011 ). sion of Enterobacteriaceae and other relatively minor mem- The inter-organismal associations within the holobiont bers of the microbiome was also observed. appear to be co-evolved and are quite dynamic. Throughout Recently, genomes of representative members of their lifetime, corals can expel or lose their dinofl agellate Oceanospirillales isolated from coral surfaces were symbionts and acquire new strains (or even clades) of sequenced. Analysis of the genome of Halomonas sp . strain Symbiodinium (Cunning et al. 2015 ). This fl exibility allows R1t3 recovered from healthy mucus of A . palmata revealed for associations with clades that may be more effective under that it belongs to the Group 2 of the polyphyletic family ever- changing environmental conditions , which may aid in Halomonadaceae (Meyer et al. 2015 ). The small subunit the holobiont’s response to environmental stressors . ribosomal RNA gene sequence of Halomonas strain R1t3 is The evidence presented in this chapter also suggests that nearly indistinguishable from the sequence in type strains of coral’s associations with bacteria are similarly co-evolved. both H. meridiana and H. aquamarina , while secA , atpA , Studies now show that microbial communities associated and rpoD are approximately 99 % identical between the two with healthy corals are not as diverse as communities associ- type strains and strain R1t3. In contrast, gene sequences for ated with diseased corals or seawater. Oceanospirillales have the gyrB locus are identical in the type strains, but only 87 % been consistently identifi ed in microbiota from stony corals similar to the gyrB locus in strain R1t3. Furthermore, small in the Caribbean , Great Barrier Reef , and the Red Sea , as subunit ribosomal RNA gene of Halomonas sp. R1t3 exhib- well as sea fans in the Mediterranean (Bourne et al. 2008 ; its high sequence identity with the orthologous genes in the Kvennefors et al. 2012 ; Littman et al. 2009 ; Pantos et al. strains RA001 (isolated from Acropora coral in India), and 2015 ; Raina et al. 2009 ; Lema et al. 2014 ; McKew et al. in the uncultured Halomonas retrieved from Acropora corals 2012 ; Meyer et al. 2014 ; Morrow et al. 2012 ; Rodriguez- in Mexico and Indonesia (Meyer et al. 2015 ). Lanetty et al. 2013 ; Sharp et al. 2012 ; Bayer et al. 2013 ; The genome of the strain R1t3 provides the fi rst glimpse Vezzulli et al. 2013 ). This specifi city suggests that the coral into the functions that are present in this coral commensal . host selects Oceanospirillales symbionts from a pool of Similarly to other halomonads, strain R1t3 tolerates a wide potential colonizers in a more directed fashion than simply range of salinities, and this is likely due to the production of setting up a competitive environment with winners that arise osmoprotectants, such as glycine betaine and ectoine. The stochastically. However, they establish within coral surface strain is able to utilize a wide range of carbon sources microbiome with time, as Oceanospirillales do not dominate (Krediet et al. 2009a , b ), and this ability is also refl ected in its microbiomes of coral larvae. Nevertheless, these associa- genome, which includes six homologues of various glyco- tions are established at very early stages of larval develop- side hydrolases predicted to act on polysaccharides, such as ment . For example, in the brooding coral , Porites astreoides , starch, glycogen, and fructan (Meyer et al. 2015 ). Oceanospirillales were detected just 4 days after larval Interestingly, whole- genome comparisons of Halomonas release (Sharp et al. 2012 ). In the broadcast spawning coral, strain R1t3 and Endozoicomonas montiporae LMG 24815 Acropora millepora , Oceanospirillales were detected in (another coral commensal ) revealed that the two genomes 1-week old juveniles , but not in planulae (Sharp et al. 2010 ). share only 392 genes (11 % of the Halomonas genome ) using These studies support earlier fi ndings that bacteria are not 60 % sequence identity and 70 % coverage criteria, or 442 associated with eggs released by several different genera and genes (12.5 % of the Halomonas genome, if 30 % sequence species of broadcast spawners, but are acquired post- similarity criterion was used).