The effect of bacteria on planula-larvae settlement and metamorphosis in the octocoral Rhytisma fulvum fulvum

Autoři: Isabel Freire aff001;  Eldad Gutner-Hoch aff002;  Andrea Muras aff001;  Yehuda Benayahu aff003;  Ana Otero aff001
Působiště autorů: Instituto de Acuicultura and Departamento de Microbiología, Facultad de Biología, Edificio CIBUS, Universidade de Santiago de Compostela, Santiago de Compostela, SPAIN aff001;  School of Zoology, George S. Wise Faculty of Life Sciences, Tel–Aviv University, Ramat-Aviv, Tel-Aviv, Israel aff002;  Interuniversity Institute for Marine Sciences, Eilat, Israel aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223214


While increasing evidence supports a key role of bacteria in coral larvae settlement and development, the relative importance of environmentally-acquired versus vertically-transferred bacterial population is not clear. Here we have attempted to elucidate the role of post-brooding-acquired bacteria on the development of planula-larvae of the octocoral Rhytisma f. fulvum, in an in vitro cultivation system employing different types of filtered (FSW) and autoclaved (ASW) seawater and with the addition of native bacteria. A good development of larvae was obtained in polystyrene 6-well cell culture plates in the absence of natural reef substrata, achieving a 60–80% of larvae entering metamorphosis after 32 days, even in bacteria-free seawater, indicating that the bacteria acquired during the brooding period are sufficient to support planulae development. No significant difference in planulae attachment and 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 bacteria. Autoclaving the different FSW homogenized the development of the larvae among the different treatments. The addition of bacterial strains isolated from the different FSW did not cause any significant effect on planulae development, although some specific strains of the genus Alteromonas seem to be beneficial for larvae development. Light was beneficial 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 beneficial phototrophic bacteria in the coral microbiome. The feasibility of obtaining advanced metamorphosed larvae in sterilized water provides an invaluable tool for studying the physiological role of the bacterial symbionts in the coral holobiont and the specificity of bacteria-coral interactions.

Klíčová slova:

Bacteria – Coral reefs – Corals – Larvae – Metamorphosis – Sea water – Insect metamorphosis – Autoclaving


1. Wilkinson C R. Global change and coral reefs: impacts on reefs, economies and human cultures. Glob Chang Biol. 1996; 2: 547–558.

2. Glynn PW. Coral reef bleaching: ecological perspectives. Coral Reefs. 1993; 12: 1–17.

3. Bryant D, Burke L, McManus JW, Spalding M. Reefs at Risk: A Map-Based Indicator of Potential Threats to the World’s Coral Reefs. (World Resources Institute). 1998.

4. Osinga R, Schutter M. Griffioen B, Wijffels RH, Verreth JAJ, Shafil S, et al. The biology and economics of coral growth. Mar Biotechnol. 2011; 13: 658–671. doi: 10.1007/s10126-011-9382-7 21584662

5. Leal MC, Calado R, Sheridan C, Alimonti A, Osinga R. Coral aquaculture to support drug discovery. Trends Biotechnol. 2013; 31: 555–561. doi: 10.1016/j.tibtech.2013.06.004 23866840

6. Rocha J, Peixe L, Gomes NCM, Calado R. Cnidarians as a source of new marine bioactive compounds—An overview of the last decade and future steps for bioprospecting. Mar Drugs. 2011; 9: 1860–1886. doi: 10.3390/md9101860 22073000

7. Mayer MA, Rodríguez DA, Taglialatela-Scafati O, Fusetani N. Marine Pharmacology in 2009–2011: Marine Compounds with Antibacterial, Antidiabetic, Antifungal, Anti-Inflammatory, Antiprotozoal, Antituberculosis, and Antiviral Activities; Affecting the Immune and Nervous Systems, and other Miscellaneous Mechanisms of action. Marine Drugs. 2013; 11: 2510–2573. doi: 10.3390/md11072510 23880931

8. Dobretsov S, Al-Wahaibi ASM, Lai D, Al-Sabahi J, Claerreboudt M, Proksch P, et al. Inhibition of bacterial fouling by soft coral natural products. Int Biodeterior Biodegrad. 2015; 98: 53–58.

9. Perkol-Finkel S, Benayahu Y. Community structure of stony and soft corals on vertical unplanned artificial reefs in Eilat (Red Sea): Comparison to natural reefs. Coral Reefs. 2004; 23: 195–205.

10. Young CN, Schopmeyer SA, Lirman D. A review of reef restoration and Coral propagation using the threatened genus Acropora in the Caribbean and western Atlantic. Bull Ma. Sci. 2012; 88: 1075–1098.

11. Bourne DG, Morrow KM, Webster NS. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev Microbiol. 2016; 70: 317–340. doi: 10.1146/annurev-micro-102215-095440 27482741

12. Thompson JR, Rivera HE, Closek CJ, Medina M. Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Front Cell Infect Microbiol. 2014; 4: 176. doi: 10.3389/fcimb.2014.00176 25621279

13. Peixoto RS, Rosado PM, Leite DC de A, Rosado AS, Bourne DG. Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front Microbiol. 2017; 8: 341. doi: 10.3389/fmicb.2017.00341 28326066

14. Weis VM, Davy SK, Hoegh-Guldberg O, Rodriguez-Lanetty M, Pringle JR. Cell biology in model systems as the key to understanding corals. Trends Ecol Evol. 2008; 23: 369–376. doi: 10.1016/j.tree.2008.03.004 18501991

15. Weber M, Medina M. The role of microalgal symbionts (Symbiodinium) inholobiont physiology. In: Piganeau G, editor. Genomic Insights Into The Biology of Algaelogy of Algae. 2012; 119–140.

16. Blackall LL, Wilson B, Van Oppen MJH. Coral—the world’s most diverse symbiotic ecosystem. Mol Ecol. 2015; 24: 5330–5347. doi: 10.1111/mec.13400 26414414

17. Rosenberg E, Kushmaro A, Kramarsky-Winter E, Banin E, Yossi L. The role of microorganisms in coral bleaching. ISME J. 2008; 3: 139–146. doi: 10.1038/ismej.2008.104 19005495

18. Sweet MJ, Bulling MT. On the importance of the microbiome and pathobiome in coral health and disease. Front Mar Sci. 2017; 4: 9.

19. Hester ER, Barott KL, Nulton J, Vermeij MJA, Rohwer FL. Stable and sporadic symbiotic communities of coral and algal holobionts. ISME J. 2015; 10: 1157–1169. doi: 10.1038/ismej.2015.190 26555246

20. Teplitski M., Krediet C. J., Meyer J. L. & Ritchie K. B. Microbial interactions on coral surfaces and within the coral holobiont BT. In: Goffredo S, Dubinsky Z, editors. The Cnidaria, Past, Present and Future: The World of Medusa and Her Sisters. Springer International Publishing. 2016; 331–346.

21. Hernandez-Agreda A, Gates RD, Ainsworth TD. Defining the core microbiome in corals’ microbial soup. Trends Microbiol. 2017; 25: 125–140. doi: 10.1016/j.tim.2016.11.003 27919551

22. van de Water JAJM, Allemand D, Ferrier-Pagès C. Host-microbe interactions in octocoral holobionts—recent advances and perspectives. Microbiome. 2018; 6: 64. doi: 10.1186/s40168-018-0431-6 29609655

23. Leah R, Omry K, Yossi L, Ilana ZR, Eugene R. The coral probiotic hypothesis. Environ Microbiol. 2006; 8: 2068–2073. doi: 10.1111/j.1462-2920.2006.01148.x 17107548

24. Rädecker N, Pogoreutz C, Voolstra CR, Wiedenmann J, Wild C. Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol. 2015; 23: 490–497. doi: 10.1016/j.tim.2015.03.008 25868684

25. Kvennefors ECE, Sampayo E, Kerr C, Vieira G, Roff G, Barnes AC. Regulation of bacterial communities through antimicrobial activity by the coral holobiont. Microb Ecol. 2012; 63: 605–618. doi: 10.1007/s00248-011-9946-0 21984347

26. Kitamura M, Koyama T, Nakano Y, Uemura D. Characterization of a natural inducer of coral larval metamorphosis. J Exp Mar Bio Ecol. 2007; 340: 96–102.

27. Tebben J, Motti CA, Siboni N, Tapiolas DM, Negri AP, Schupp PJ, et al. Chemical mediation of coral larval settlement by crustose coralline algae. Sci Rep. 2015; 5: 1–11.

28. Benayahu Y, Loya Y. Substratum preferences and planulae settling of two red sea alcyonaceans: Xenia macrospiculata Gohar and Parerythropodium fulvum fulvum (Forskl). J Exp Mar Biol Ecol. 1984; 83: 249–260

29. Negri AP, Webster NS, Hill RT, Heyward AJ. Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar Ecol Prog Ser. 2001; 223: 121–131.

30. Tebben J, Tapiolas DM, Motti CA, Abrego D, Negri AP, Blackall LL, et al. Induction of larval metamorphosis of the coral Acropora millepora by tetrabromopyrrole isolated from a Pseudoalteromonas bacterium. PLoS One. 2011; 6: e19082. doi: 10.1371/journal.pone.0019082 21559509

31. Ritson-Williams R, Paul VJ, Arnold SN, Steneck RS. Larval settlement preferences and post-settlement survival of the threatened Caribbean corals Acropora palmata and A. cervicornis. Coral Reefs. 2010; 29: 71–81.

32. Webster NS, Smith LD, Heyward AJ, Watts JE, Webb RI, Blackall LL, et al. Metamorphosis of a Scleractinian Coral in Response to Microbial Biofilms. Appl Environ Microbiol. 2004; 70: 1213–1221. doi: 10.1128/AEM.70.2.1213-1221.2004 14766608

33. Unabia CRC, Hadfield MG Role of bacteria in larval settlement and metamorphosis of the polychaete Hydroides elegans. Mar Biol. 1999; 133: 55–64.

34. Karen T, Jon H. Investigating a possible role for the bacterial signal molecules N-acylhomoserine lactones in Balanus improvisus cyprid settlement. Mol Ecol. 2013; 22: 2588–2602. doi: 10.1111/mec.12273 23506419

35. Ben-David-Zaslow R, Benayahu Y. Competence and longevity in planulae of several soft corals. Mar. Ecol. Ser. 1998; 171: 235–243.

36. Hadfield MG. Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. Ann Rev Mar Sci. 011; 3: 453–470.

37. Freckelton ML, Nedved BT, Hadfield MG. Induction of invertebrate larval settlement; different bacteria, different mechanisms? Sci Rep. 2017; 7: 42557. doi: 10.1038/srep42557 28195220

38. Hadfield M. & Paul V. Natural Chemical Cues for Settlement and Metamorphosis of Marine-Invertebrate Larvae. In: McClinctock JB, Baker BJ. Marine Chemical Ecology. 2001; 431–461.

39. Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N. Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 2001; 20: 85–91.

40. Ceh J, Raina JB, Soo RM, van Keulen M, Bourne DG. Coral-bacterial communities before and after a coral mass spawning event on Ningaloo Reef. PLoS One. 2012; 7: e36920. doi: 10.1371/journal.pone.0036920 22629343

41. Sharp KH, Distel D, Paul VJ. Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides. ISME J. 2012, 6: 790–801. doi: 10.1038/ismej.2011.144 22113375

42. Ceh J, van Keulen M, Bourne DG. Intergenerational transfer of specific bacteria in corals and possible implications for offspring fitness. Microb Ecol. 2013; 65: 227–231. doi: 10.1007/s00248-012-0105-z 22895828

43. Apprill A, Marlow HQ, Martindale MQ, Rappé MS. The onset of microbial associations in the coral Pocillopora meandrina. ISME J. 2009; 3: 685. doi: 10.1038/ismej.2009.3 19242535

44. Leite DCA, Leao P, Garrido AG, Lins U, Santos HF, Pires DO, et al. Broadcast spawning coral Mussismilia hispida can vertically transfer its associated bacterial core. Front Microbiol. 2017; 8: 176. doi: 10.3389/fmicb.2017.00176 28223979

45. Sharp KH, Ritchie KB, Schupp PJ, Ritson-Williams R, Paul VJ. Bacterial acquisition in juveniles of several broadcast spawning coral species. PLoS One. 2010; 5: e10898. doi: 10.1371/journal.pone.0010898 20526374

46. Slattery M, Hines GA, Starmer J, Paul VJ. Chemical signals in gametogenesis, spawning, and larval settlement and defense of the soft coral Sinularia polydactyla. Coral Reefs. 1999; 18: 75–84.

47. Benayahu Y, Loya Y. Surface brooding in the Red Sea soft coral Parerythropodium fulvum fulvum (FORSKÅL, 1775). Biol Bull. 1983; 165: 353–369. doi: 10.2307/1541201 28368228

48. Tait K, Joint I, Daykin M, Milton DL, Williams P, Cámara M. Disruption of quorum sensing in seawater abolishes attraction of zoospores of the green alga Ulva to bacterial biofilms. Environ Microbiol. 2005; 7: 229–240. doi: 10.1111/j.1462-2920.2004.00706.x 15658990

49. Mühling M, Woolven-Allen J, Murrell JC, Joint I. Improved group-specific PCR primers for denaturing gradient gel electrophoresis analysis of the genetic diversity of complex microbial communities. ISME J. 2008; 2: 379. doi: 10.1038/ismej.2007.97 18340335

50. Twigg MS, Tait K, Williams P, Atkinson S, Cámara M. Interference with the germination and growth of Ulva zoospores by quorum-sensing molecules from Ulva-associated epiphytic bacteria. Environ Microbiol. 2014; 16: 445–453. doi: 10.1111/1462-2920.12203 23879807

51. Zeileis A, Wiel MA van de, Hornik K, Hothorn T. Implementing a class of permutation tests: the coin package. J. Stat. Softw. 2008; 28. doi: 10.18637/jss.v028.i07

52. Tran C, Hadfield MG Larvae of Pocillopora damicornis (Anthozoa) settle and metamorphose in response to surface-biofilm bacteria. Mar Ecol Prog Ser. 2011; 433: 85–96.

53. Sneed JM, Sharp KH, Ritchie KB, Paul VJ. The chemical cue tetrabromopyrrole from a biofilm bacterium induces settlement of multiple Caribbean corals. Proc R Soc B Biol Sci. 2014; 281: 20133086.

54. Huang YL, Ki JS, Lee OO, Qian PY. Evidence for the dynamics of Acyl homoserine lactone and AHL-producing bacteria during subtidal biofilm formation. ISME J. 2008; 3: 296–304. doi: 10.1038/ismej.2008.105 18987676

55. Kelman D, Kushmaro A, Loya Y, Kashman Y, Benayahu Y. Antimicrobial activity of a Red Sea soft coral, Parerythropodium fulvum fulvum: Reproductive and developmental considerations. Mar Ecol Prog Ser. 1998; 169: 87–95.

56. Mundy CN, Babcock RC. Role of light intensity and spectral quality in coral settlement: Implications for depth-dependent settlement? J Exp Mar Bio Ecol. 1998, 223: 235–255.

57. Vermeij MJA, Smith JE, Smith CM, Vega Thurber R, Sandin SA. Survival and settlement success of coral planulae: independent and synergistic effects of macroalgae and microbes. Oecologia. 2009; 159: 325–336. doi: 10.1007/s00442-008-1223-7 19050932

58. Tinh NT, Asanka Gunasekara RA, Boon N, Dierckens K, Sorgeloos P, Bossier P. N-acyl homoserine lactone-degrading microbial enrichment cultures isolated from Penaeus vannamei shrimp gut and their probiotic properties in Brachionus plicatilis cultures. FEMS Microbiol Ecol. 2007; 62: 45–53. doi: 10.1111/j.1574-6941.2007.00378.x 17784866

59. Shnit-Orland M, Kushmaro A. Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol. 2009, 67: 371–380. doi: 10.1111/j.1574-6941.2008.00644.x 19161430

60. Lemos ML, Dopazo CP, Toranzo A, Barja JL. Competitive dominance of antibiotic-producing marine bacteria in mixed cultures. J Appl Bacteriol. 1991; 71: 228–232. doi: 10.1111/j.1365-2672.1991.tb04452.x 1955417

Článek vyšel v časopise


2019 Číslo 9

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Zvyšte si kvalifikaci online z pohodlí domova

Antiseptika a prevence ve stomatologii
nový kurz
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Citikolin v neuroprotekci a neuroregeneraci: od výzkumu do klinické praxe nejen očních lékařů
Autoři: MUDr. Petr Výborný, CSc., FEBO

Zánětlivá bolest zad a axiální spondylartritida – Diagnostika a referenční strategie
Autoři: MUDr. Monika Gregová, Ph.D., MUDr. Kristýna Bubová

Diagnostika a léčba deprese pro ambulantní praxi
Autoři: MUDr. Jan Hubeňák, Ph.D

Význam nemocničního alert systému v době SARS-CoV-2
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D., prim. MUDr. Václava Adámková

Všechny kurzy
Kurzy Doporučená témata