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The Effect of Bacteria on Planula-Larvae Settlement and Metamorphosis in the Octocoral Rhytisma Fulvum Fulvum

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The Effect of Bacteria on Planula-Larvae Settlement and Metamorphosis in the Octocoral Rhytisma Fulvum Fulvum See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/336145787 The effect of bacteria on planula-larvae settlement and metamorphosis in the octocoral Rhytisma fulvum fulvum Article in PLoS ONE · September 2019 DOI: 10.1371/journal.pone.0223214 CITATIONS READS 0 54 5 authors, including: Isabel Freire Eldad Gutner-Hoch University of Santiago de Compostela Marine Biological Laboratory 4 PUBLICATIONS 14 CITATIONS 19 PUBLICATIONS 72 CITATIONS SEE PROFILE SEE PROFILE Andrea Muras Yehuda Benayahu University of Santiago de Compostela Tel Aviv University 15 PUBLICATIONS 87 CITATIONS 264 PUBLICATIONS 5,866 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: BYEFOULING View project BYEFOULING View project All content following this page was uploaded by Eldad Gutner-Hoch on 09 October 2019. The user has requested enhancement of the downloaded file. RESEARCH ARTICLE The effect of bacteria on planula-larvae settlement and metamorphosis in the octocoral Rhytisma fulvum fulvum 1 2¤ 1 3 1 Isabel Freire , Eldad Gutner-Hoch , Andrea Muras , Yehuda Benayahu , Ana OteroID * 1 Instituto de Acuicultura and Departamento de MicrobiologõÂa, Facultad de BiologõÂa, Edificio CIBUS, Universidade de Santiago de Compostela, Santiago de Compostela, SPAIN, 2 School of Zoology, George S. Wise Faculty of Life Sciences, Tel±Aviv University, Ramat-Aviv, Tel-Aviv, Israel, 3 Interuniversity Institute for a1111111111 Marine Sciences, Eilat, Israel a1111111111 a1111111111 ¤ Current address: The Eugene Bell Center, Marine Biological Laboratory, Woods Hole, Ma, United States of America a1111111111 * [email protected] a1111111111 Abstract OPEN ACCESS While increasing evidence supports a key role of bacteria in coral larvae settlement and development, the relative importance of environmentally-acquired versus vertically-trans- Citation: Freire I, Gutner-Hoch E, Muras A, Benayahu Y, Otero A (2019) The effect of bacteria ferred bacterial population is not clear. Here we have attempted to elucidate the role of post- on planula-larvae settlement and metamorphosis in brooding-acquired bacteria on the development of planula-larvae of the octocoral Rhytisma the octocoral Rhytisma fulvum fulvum. PLoS ONE f. fulvum, in an in vitro cultivation system employing different types of filtered (FSW) and 14(9): e0223214. https://doi.org/10.1371/journal. autoclaved (ASW) seawater and with the addition of native bacteria. A good development of pone.0223214 larvae was obtained in polystyrene 6-well cell culture plates in the absence of natural reef Editor: Hector Escriva, Laboratoire Arago, FRANCE substrata, achieving a 60±80% of larvae entering metamorphosis after 32 days, even in bac- Received: June 18, 2019 teria-free seawater, indicating that the bacteria acquired during the brooding period are suffi- Accepted: September 16, 2019 cient to support planulae development. No significant difference in planulae attachment and Published: September 30, 2019 development was observed when using 0.45 μm or 0.22 μm FSW, although autoclaving the 0.45 μm FSW negatively affected larval development, indicating the presence of beneficial Peer Review History: PLOS recognizes the benefits of transparency in the peer review bacteria. Autoclaving the different FSW homogenized the development of the larvae among process; therefore, we enable the publication of the different treatments. The addition of bacterial strains isolated from the different FSW did all of the content of peer review and author not cause any significant effect on planulae development, although some specific strains of responses alongside final, published articles. The the genus Alteromonas seem to be beneficial for larvae development. Light was beneficial editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0223214 for planulae development after day 20, although no Symbiodinium cells could be observed, indicating either that light acts as a positive cue for larval development or the presence of Copyright: © 2019 Freire et al. This is an open access article distributed under the terms of the beneficial phototrophic bacteria in the coral microbiome. The feasibility of obtaining Creative Commons Attribution License, which advanced metamorphosed larvae in sterilized water provides an invaluable tool for studying permits unrestricted use, distribution, and the physiological role of the bacterial symbionts in the coral holobiont and the specificity of reproduction in any medium, provided the original author and source are credited. bacteria-coral interactions. Data Availability Statement: All relevant data are within the manuscript and its Supporting Information files. Funding: This work was supported by: EU FP7- Research Infrastructure Initiative Assemble PLOS ONE | https://doi.org/10.1371/journal.pone.0223214 September 30, 2019 1 / 18 Effect of bacteria on R. fulvum fulvum planulae (Association of European marine biological Introduction laboratories); EU FP7 Project Byefouling (grant agreement no 612717); Xunta de Galicia, Coral reefs are suffering substantial degradation at a global scale [1]. It is estimated that ~60% ConsellerõÂa de Cultura, EducacioÂn e OrdenacioÂn of the reefs are already daged either directly as the result of human activities or indirectly by Universitaria (grant number ED431D 2017/22). The factors derived from global climate change, such as ocean acidification and changes in temper- funders had no role in study design, data collection ature, salinity, or light [2±3]. In addition to their ecological significance, coral reefs constitute and analysis, decision to publish, or preparation of an invaluable economic resource, with plethora of natural products of biotechnological and the manuscript. pharmaceutical interest having been isolated from reef organisms, featuring anti-cancer, anti- Competing interests: The authors have declared microbial, anti-viral and anti-inflammatory properties [4±8]. Consequently, establishing in- that no competing interests exist. vitro cultivation systems that will allow the identification of the factors that determine the suc- cessful settlement and development of coral planulae-larvae is of prime importance to the on- going world-wide efforts for reef conservation [9±10]. One of the key aspects in coral life cycle and development is that of the interaction with their associated microorganisms. The coral holobiont is a complex symbiotic system that encompasses symbiotic dinoflagellate algae, bacteria, fungi, viruses, and other protists [11±13]. However, while the symbiotic relationship between the endosymbiotic dinoflagellate algae (zooxanthellae) and their coral host has been studied in depth [11, 14±16], the complex mecha- nisms controlling coral-bacteria interactions are still poorly understood. In particular, the specificity of the coral-bacteria association remains unclear, despite numerous studies having indicated a crucial role of bacteria for the well-being of corals [17±18]. High-throughput sequencing techniques have revealed the high bacterial diversity harboured by adult corals, with an increasing evidence of the existence of a species-specific ªcore microbiomeº that seems to be regulated by the host through different mechanisms [19±22]. The coral probiotic theory [23], has led to the term "Beneficial Microorganisms for Corals" (BMCs) being coined, aimed at defining the specific bacterial symbionts that may promote coral health, and thus be of potential use as environmental probiotics to reverse dysbiosis [13]. The potential functions of this beneficial microbiota include carbon, nitrogen and sulphur cycling [24], as well as the production of anti-microbial compounds [25], thereby facilitating pathogen control. Since the settlement and metamorphosis of coral planula-larvae are known to be governed by environmental cues, several studies have examined the role of bacteria in these processes, mainly for stony coral species. The best-known source of chemical morphogens for coral plan- ulae are the crustaceous coralline algae (CCA) [26±28]. However, the nature of the biochemical cues present in CCA is not clear and may be partially derived from the presence of epiphytic bacteria [29]. Bacterial biofilms also produce cues for the settlement process that can be recog- nised by planulae [29±32], as previously reported for various marine invertebrates [33±34]. Indeed, the addition of antibiotics has been shown to block settlement and development in several Octocorallia species [35]. The nature of the biochemical and/or physical cues present in microbial biofilms remains elusive [36±37]. In many cases the percentage of settlement induced by monospecific bacterial strains was lower than that resulting from natural, multispe- cies films [32±33]. It is however possible that specific types of bacteria may be responsible for facilitating settlement and metamorphosis [36±38]. Members of the Roseobacter clade, a group frequently associated with stony corals [39], have been found to be constantly present in their planula-larvae [40±42], constituting up to 70% of the SSU rDNA sequences obtained [43]. Bacteria belonging to the genera Alteromonas, Shewanella and Marinobacter have also been associated with planulae or coral gametes in stony corals [41±42]. In other cases, mem- bers of the genera Burkholderia, Pseudomonas, Acinetobacter, Ralstonia and Bacillus have been reported to be transmitted vertically to their gametes [44]. A number
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