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Induction of Larval Settlement in the Reef Coral Porites Astreoides by a Cultivated Marine Roseobacter Strain

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Induction of Larval Settlement in the Reef Coral Porites Astreoides by a Cultivated Marine Roseobacter Strain View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by DOCS@RWU Roger Williams University DOCS@RWU Arts & Sciences Faculty Publications Arts and Sciences 2015 Induction of Larval Settlement in the Reef Coral Porites astreoides by a Cultivated Marine Roseobacter Strain Koty H. Sharp Roger Williams University, [email protected] Follow this and additional works at: https://docs.rwu.edu/fcas_fp Part of the Biology Commons, and the Marine Biology Commons Recommended Citation Sharp,K.H., Sneed, J.M., Ritchie, K.B., McDaniel, L., & Paul, V. J. (2015). Induction of larval settlement in the reef coral porites astreoides by a cultivated marine roseobacter strain. The Biological Bulletin 228, 98-107. This Article is brought to you for free and open access by the Arts and Sciences at DOCS@RWU. It has been accepted for inclusion in Arts & Sciences Faculty Publications by an authorized administrator of DOCS@RWU. For more information, please contact [email protected]. Reference: Biol. Bull. 228: 98–107. (April 2015) © 2015 Marine Biological Laboratory Induction of Larval Settlement in the Reef Coral Porites astreoides by a Cultivated Marine Roseobacter Strain K. H. SHARP1*, J. M. SNEED2, K. B. RITCHIE3, L. MCDANIEL4, AND V. J. PAUL2 1Eckerd College, 4200 54th Avenue South, St. Petersburg, Florida 33711; 2Smithsonian Marine Station, 701 Seaway Drive, Fort Pierce, Florida 34949; 3Mote Marine Laboratory, 1600 Ken Thompson Pkwy, Sarasota, Florida 34236; and 4University of South Florida College of Marine Science, 140 7th Avenue S., St. Petersburg, Florida 33701 Abstract. Successful larval settlement and recruitment naturally occurring, complex microbial biofilms on reef by corals is critical for the survival of coral reef ecosystems. surfaces. Several closely related strains of ␥-proteobacteria have been identified as cues for coral larval settlement, but the induc- Introduction tive properties of other bacterial taxa naturally occurring in The settlement, survival, and growth of coral larvae play reef ecosystems have not yet been explored. In this study, a critical role in the resilience and repopulation of coral reef we assayed bacterial strains representing taxonomic groups ecosystems (Hughes et al., 2003). The ultimate settlement consistently detected in corals for their ability to influence and post-settlement survival of coral larvae is regulated by larval settlement in the coral Porites astreoides. We iden- several biotic and abiotic factors, including availability of tified one ␣-proteobacterial strain, Roseivivax sp. 46E8, suitable substrate for settlement. Various surfaces in the reef which significantly increased larval settlement in P. as- environment have differential effects on larval settlement. treoides. Logarithmic growth phase (log phase) cell cultures Larval recruitment rates are lower in areas with abundant of Roseivivax sp. 46E8 and filtrates (0.22␮m) from log macroalgae (Edmunds and Carpenter, 2001) due to allelo- phase Roseivivax sp. 46E8 cultures significantly increased pathic compounds produced by macroalgae (Kuffner and settlement, suggesting that an extracellular settlement factor Paul, 2004; Birrell et al., 2005, 2008; Kuffner et al., 2006; is produced during active growth phase. Filtrates from log Ritson-Williams et al., 2009, 2010; Paul et al., 2011). phase cultures of two other bacterial isolates, Marinobacter Recent evidence also suggests that macroalgae can shape sp. 46E3, and Cytophaga sp. 46B6, also significantly in- the bacterial community composition in the benthos (Barott creased settlement, but the cell cultures themselves did not. et al., 2011; Morrow et al., 2012; Vega Thurber et al., Monospecific biofilms of the three strains did not result in 2012). In contrast, other algal species, including particular significant increases in larval settlement. Organic and aque- species of crustose coralline algae (CCA) (Ritson-Williams ous/methanol extracts of Roseivivax sp. 46E8 cultures did et al., 2010, 2014) and compounds derived from CCA not affect larval settlement. Examination of filtrates from (Kitamura et al., 2007, 2009) facilitate larval settlement of cell cultures showed that Roseivivax sp. 46E8 spontane- scleractinian corals. ously generated virus-like particles in log and stationary The positive influence of specific surfaces in the marine phase growth. Though the mechanism of settlement en- environment on larval settlement is likely due to a combi- hancement by Roseivivax sp. 46E8 is not yet elucidated, our nation of microbe-microbe interactions within surface bio- findings point to a new aspect of coral-Roseobacter inter- films, physical factors of the benthic environment on a actions that should be further investigated, especially in microscopic scale, and the production of chemical cues. Bacteria in multi-species biofilms on surfaces in benthic Received 29 August 2014; accepted 12 March 2015. ecosystems influence settlement in diverse marine inverte- * To whom correspondence should be addressed. E-mail: brate phyla (reviewed in Hadfield, 2011). Successful settle- [email protected] ment of invertebrate larvae (attachment and metamorphosis) 98 This content downloaded from 198.007.243.146 on October 25, 2019 06:21:02 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). ROSEOBACTER AND CORAL SETTLEMENT 99 is strongly governed by the density, taxonomic composition, (Nissimov et al., 2009); or metabolize dimethylsulfoniopro- and activity of bacteria in reef environments (Huang and pionate (DMSP) (Raina et al., 2009, 2010; Bourne et al., Hadfield, 2003). Marhaver et al. (2013) showed that ma- 2013). Roseobacter bacteria are among the main taxonomic nipulation of microbes in reef seawater influences coral groups consistently associated with cnidarian-associated larval settlement and survival and, ultimately, the large- Symbiodinium spp. In addition, bacteria from the genera scale landscape of coral reefs. A specific strain from the Marinobacter and Cytophaga are consistently associated genus Pseudoalteromonas, cultured from the surface of the with Symbiodinium (Ritchie, 2011). CCA Neogoniolithon fosliei, produces the small molecule In this study, we explored the ability of three bacterial tetrabromopyrrole (TBP) that induces metamorphosis but strains, Roseivivax sp. 46E8, Marinobacter sp. 46E3, and not attachment in the Pacific coral Acropora millepora Cytophaga sp. 46B6, isolated from a collection of Symbio- (Tebben et al., 2011; Siboni et al., 2012, 2014). However, a dinium spp. cultures, to influence larval settlement in the closely related strain of Pseudoalteromonas sp., cultured coral Porites astreoides Lamarck, 1816. We used P. as- from the CCA Paragoniolithon solubile, produces TBP and treoides because it is common throughout the Caribbean induces both attachment and metamorphosis in multiple and the Atlantic basin; it is robust to laboratory manipula- species of Caribbean corals (Sneed et al., 2014). In the tion; and it predictably releases large numbers of competent Pacific coral Pocillopora damicornis, strains of Pseudo- larvae on a seasonal basis. We exposed P. astreoides larvae alteromonas and Thalassomonas isolated from marine sur- to liquid cultures—both logarithimic and stationary growth faces also induce both metamorphosis and attachment (Tran phase—and monospecific biofilms of the three bacterial and Hadfield, 2011). Inductive capabilities were found in strains, and we assayed them for induction of larval settle- bacteria from both genera, and in isolates from a range of ment. We also tested cell-free filtrates and organic and benthic surfaces, including macroalgae, corals, and bio- aqueous/methanol extracts of the cultures in larval settle- filmed glass slides (Tran and Hadfield, 2011), suggesting ment assays. We imaged filtrates from inductive liquid that the inductive properties are not exclusive to one genus cultures in order to test for the presence of potential induc- of bacterium nor to bacteria from particular surfaces (Tran tive particles not identified with traditional methods of and Hadfield, 2011). An additional mechanism of bacterial extracting bioactive compounds. induction of larval settlement has been recently identified. A strain of Pseudoalteromonas luteoviolacea, isolated from a Materials and Methods marine biofilm, produces arrays of contractile phage tail- like structures that induce larval settlement of the serpulid Colony collection and larval rearing worm Hydroides elegans (Shikuma et al., 2014). This find- Collection efforts were timed around the new moon in the ing demonstrates that phage-associated structures may play months of April, May, and June in 2012. Porites astreoides a role in induction of settlement although the exact mech- colonies were collected at least 24 h before the new moon anism of induction is yet unknown. from Wonderland Reef, located in the Lower Florida Keys Fluorescence in situ hybridization (FISH) with sequence- (24°33.69ЈN, 081°30.08ЈW). Colonies were transported in specific probes suggests that the most abundant groups of coolers to Mote Tropical Research Laboratory in Summer- bacteria on biofilms inductive to the coral Acropora micro- land Key, Florida, and maintained in a flow-through seawa- ␥ ␣ pthalma are -proteobacteria, -proteobacteria, and Cy- ter system. Larvae were released each night for 3–5 nights tophaga (Webster et al., 2004). However, of that described after collection. Throughout the larval release period, larvae diversity, to date, all of the cultured bacterial isolates
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