Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-20T18:29:20.350Z Has data issue: false hasContentIssue false
  • English
  • Français

Assessing the core microbial symbionts of jellyfish in Indonesian and Vietnamese marine lakes

Published online by Cambridge University Press:  12 October 2022

Marina R.S. Ferreira Open the ORCID record for Marina R.S. Ferreira [Opens in a new window] ,
Daniel F.R. Cleary Open the ORCID record for Daniel F.R. Cleary [Opens in a new window] ,
Nguyen K. Bat ,
Ana R.M. Polónia Open the ORCID record for Ana R.M. Polónia [Opens in a new window]  and
Newton C.M. Gomes Open the ORCID record for Newton C.M. Gomes [Opens in a new window]
Marina R.S. Ferreira*
Affiliation:
Department of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Campus Universitário de Santiago, 3810-193 Aveiro, Portugal
Daniel F.R. Cleary
Affiliation:
Department of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Campus Universitário de Santiago, 3810-193 Aveiro, Portugal
Nguyen K. Bat
Affiliation:
Research Institute for Marine Fisheries, 224 Le Lai, Haiphong, Vietnam
Ana R.M. Polónia
Affiliation:
Department of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Campus Universitário de Santiago, 3810-193 Aveiro, Portugal
Newton C.M. Gomes
Affiliation:
Department of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Campus Universitário de Santiago, 3810-193 Aveiro, Portugal
*
Author for correspondence: Marina R. S. Ferreira, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Jellyfish are a well-known component of marine ecosystems. Here, we aimed to assess whether populations of the jellyfish species Mastigias cf. papua and Cassiopea ornata inhabiting different marine lakes and jellyfish species from open water habitat host ‘core’ symbionts and if there is evidence of species-specific host-microbial associations. Compositionally, jellyfishes hosted prokaryotic communities distinct from those found in water samples. All jellyfish samples across habitats and species exhibited a core OTU, assigned to the genus Endozoicomonas. This OTU was particularly abundant (>90% of all sequences) in C. ornata from one Papuan marine lake. Additionally, an OTU assigned to the Entomoplasmatales order was found in all but two jellyfish specimens, and was particularly abundant in marine lake specimens from Berau and Papua, Indonesia. Given the well-known relationship between Endozoicomonas and Symbiodinium spp., we tested for Symbiodinium presence in pooled specimens of M. papua from Berau. Our results showed that OTUs assigned to the genus Symbiodinium accounted for >99% of all sequences in jellyfish-associated microeukaryotic communities; these were closely related to organisms from Symbiodinium clade C. These results suggest the existence of a widespread and abundant jellyfish core symbiont, which may interact with symbiotic Symbiodinium populations to influence host fitness.

Keywords

Anchialine systemsCassiopeaIlluminaMastigiasmicrobial composition
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 102 , Issue 7 , November 2022 , pp. 486 - 495
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Awai, K, Matsuoka, R and Shioi, Y (2012) Lipid and fatty acid compositions of Symbiodinium strains. In Proceedings of the 12th International Coral Reef Symposium.Google Scholar
Azzini, F, Calcinai, B, Cerrano, C, Bavestrello, G and Pansini, M (2007) Sponges of the marine karst lakes and of the coast of the islands of Ha Long Bay (North Vietnam). In Custodia, MR, Lobo-Hajdu, G, Hajdu, E and Muricy, G (eds), Porifera Research: Biodiversity Innovation and Sustainability. Rio de Janeiro: Museu Nacional, pp. 157–164.Google Scholar
Becking, LE, de Leeuw, C and Vogler, C (2015) Newly discovered “jellyfish lakes” in Misool, Raja Ampat, Papua, Indonesia. Marine Biodiversity 45, 597–598.CrossRefGoogle Scholar
Becking, LE, Renema, W, Santodomingo, NK, Hoeksema, BW, Tuti, Y and de Voogd, NJ (2011) Recently discovered landlocked basins in Indonesia reveal high habitat diversity in anchialine systems. Hydrobiologia 677, 89–105.CrossRefGoogle Scholar
Bernasconi, R, Stat, M, Koenders, A and Huggett, MJ (2019) Global networks of Symbiodinium-bacteria within the coral holobiont. Microbial Ecology 77, 794–807.CrossRefGoogle ScholarPubMed
Brekhman, V, Malik, A, Haas, B, Sher, N and Lotan, T (2015) Transcriptome profiling of the dynamic life cycle of the scypohozoan jellyfish Aurelia aurita. BMC Genomics 16, 1–15.CrossRefGoogle ScholarPubMed
Caporaso, JG, Kuczynski, J, Stombaugh, J, Bittinger, K, Bushman, FD, Costello, EK, Fierer, N, Peña, AG, Goodrich, JK, Gordon, JI, Huttley, GA, Kelley, ST, Knights, D, Koenig, JE, Ley, RE, Lozupone, CA, McDonald, D, Muegge, BD, Pirrung, M, Reeder, J, Sevinsky, JR, Turnbaugh, PJ, Walters, WA, Widmann, J, Yatsunenko, T, Zaneveld, J and Knight, R (2010) QIIME Allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336.CrossRefGoogle ScholarPubMed
Cerrano, C, Azzini, F, Bavestrello, G, Calcinai, B, Pansini, M, Sarti, M and Thung, D (2006) Marine lakes of karst islands in Ha Long Bay (Vietnam). Chemistry and Ecology 22, 489–500.CrossRefGoogle Scholar
Chernov, VM, Chernova, OA, Mouzykantov, AA, Medvedeva, ES, Baranova, NB, Malygina, TY, Aminov, RI and Trushin, MV (2018) Antimicrobial resistance in mollicutes: known and newly emerging mechanisms. FEMS Microbiology Letters 365, fny185.CrossRefGoogle ScholarPubMed
Cimino, MA, Patris, S, Ucharm, G, Bell, LJ and Terrill, E (2018) Jellyfish distribution and abundance in relation to the physical habitat of Jellyfish Lake, Palau. Journal of Tropical Ecology 34, 17–31.CrossRefGoogle Scholar
Cleary, DFR, Becking, LE, de Voogd, NJ, Pires, AC, Polónia, ARM, Egas, C and Gomes, NCM (2013) Habitat-and host-related variation in sponge bacterial symbiont communities in Indonesian waters. FEMS Microbiology Ecology 85, 465–482.CrossRefGoogle ScholarPubMed
Cleary, DFR, Becking, LE, Polónia, ARM, Freitas, RM and Gomes, NCM (2015) Composition and predicted functional ecology of mussel-associated bacteria in Indonesian marine lakes. Antonie van Leeuwenhoek 107, 821–834.CrossRefGoogle ScholarPubMed
Cleary, DFR, Becking, LE, Polónia, ARM, Freitas, RM and Gomes, NCM (2016) Jellyfish-associated bacterial communities and bacterioplankton in Indonesian Marine lakes. FEMS Microbiology Ecology 92, fiw064.CrossRefGoogle ScholarPubMed
Cleary, DFR, Ferreira, MRS, Bat, NK, Polónia, ARM, Gomes, NCM and de Voogd, NJ (2020) Bacterial composition of sponges, sediment and seawater in enclosed and open marine lakes in Ha Long Bay Vietnam. Marine Biology Research 16, 18–31.CrossRefGoogle Scholar
Cleary, DFR and Polónia, ARM (2018) Bacterial and archaeal communities inhabiting mussels, sediment and water in Indonesian anchialine lakes. Antonie van Leeuwenhoek 111, 237–257.CrossRefGoogle ScholarPubMed
Cleary, DFR, Polónia, ARM and de Voogd, NJ (2018) Prokaryote composition and predicted metagenomic content of two Cinachyrella morphospecies and water from West Papuan marine lakes. FEMS Microbiology Ecology 94, fix175.CrossRefGoogle ScholarPubMed
Coelho, FJRC, Cleary, DFR, Gomes, NCM, Pólonia, ARM, Huang, YM, Liu, LL and de Voogd, NJ (2018) Sponge prokaryote communities in Taiwanese coral reef and shallow hydrothermal vent ecosystems. Microbial Ecology 75, 239–254.CrossRefGoogle ScholarPubMed
Coelho, FJ, Louvado, A, Domingues, PM, Cleary, DFR, Ferreira, MRS, Almeida, A, Cunha, MR, Cunha, A and Gomes, NCM (2016) Integrated analysis of bacterial and microeukaryotic communities from differentially active mud volcanoes in the Gulf of Cadiz. Scientific Reports 6, 1–10.CrossRefGoogle ScholarPubMed
Cook, AA, Bhadury, P, Debenham, NJ, Meldal, BHM, Blaxter, ML, Smerdon, GR, Austen, MC, Lambshead, PJD and Rogers, AD (2005) Denaturing gradient gel electrophoresis (DGGE) as a tool for identification of marine nematodes. Marine Ecology Progress Series 291, 103–113.CrossRefGoogle Scholar
Costa, R, Keller-Costa, T, Gomes, NC, da Rocha, UN, van Overbeek, L and van Elsas, JD (2013) Evidence for selective bacterial community structuring in the freshwater sponge Ephydatia fluviatilis. Applied and Environmental Microbiology 76, 232–244.Google Scholar
Daley, MC, Urban-Rich, J and Moisander, PH (2016) Bacterial associations with the hydromedusa Nemopsis bachei and scyphomedusa Aurelia aurita from the North Atlantic Ocean. Marine Biology Research 12, 1088–1100.CrossRefGoogle Scholar
Dawson, MN (2005 a) Five new subspecies of Mastigias (Scyphozoa: Rhizostomeae: Mastigiidae) from marine lakes, Palau, Micronesia. Journal of the Marine Biological Association of the United Kingdom 85, 679–694.CrossRefGoogle Scholar
Dawson, MN (2005 b) Morphological variation and systematics in the Scyphozoa: Mastigias (Rhizostomeae, Mastigiidae) – a golden unstandard? Hydrobiologia 537, 185–206.CrossRefGoogle Scholar
Dawson, MN, Martin, LE and Penland, LK (2001) Jellyfish swarms, tourists, and the Christ-child. In Jellyfish Blooms: Ecological and Societal Importance. Dordrecht: Springer, pp. 131–144.CrossRefGoogle Scholar
Edgar, RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10, 996–998.CrossRefGoogle ScholarPubMed
Fonseca, VG, Carvalho, GR, Sung, W, Johnson, HF, Power, DM, Neill, SP, Packer, M, Blaxter, ML, Lambshead, PJD, Thomas, WK and Creer, S (2010) Second-generation environmental sequencing unmasks marine metazoan biodiversity. Nature Communications 1, 1–8.CrossRefGoogle ScholarPubMed
Freeman, CJ, Stoner, EW, Easson, CG, Matterson, KO and Baker, DM (2017) Variation in δ13C and δ15N values suggests a coupling of host and symbiont metabolism in the Symbiodinium–Cassiopea mutualism. Marine Ecology Progress Series 571, 245–251.CrossRefGoogle Scholar
Hamner, WM, Gilmer, RW and Hamner, PP (1982) The physical, chemical, and biological characteristics of a stratified, saline, sulfide lake in Palau 1. Limnology and Oceanography 27, 896–909.CrossRefGoogle Scholar
Hamner, WM and Hauri, IR (1981) Effects of island mass: water flow and plankton pattern around a reef in the Great Barrier Reef lagoon, Australia 1. Limnology and Oceanography 26, 1084–1102.CrossRefGoogle Scholar
Kawabata, T, Lindsay, DJ, Kitamura, M, Konishi, S, Nishikawa, J, Nishida, S, Kamio, M and Nagai, H (2013) Evaluation of the bioactivities of water-soluble extracts from twelve deep-sea jellyfish species. Fisheries Science 79, 487–494.CrossRefGoogle Scholar
Klein, SG, Pitt, KA, Nitschke, MR, Goyen, S, Welsh, DT, Suggett, DJ and Carroll, AR (2017) Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian. Global Change Biology 23, 3690–3703.CrossRefGoogle ScholarPubMed
Klindworth, A, Pruesse, E, Schweer, T, Peplies, J, Quast, C, Horn, M and Glöckner, FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Applied and Environmental Microbiology 76, e1.Google Scholar
Kramar, MK, Tinta, T, Lučić, D, Malej, A and Turk, V (2018) Bacteria associated with jellyfish during bloom and post-bloom periods. bioRxiv, 329524.CrossRefGoogle Scholar
Kramar, MK, Tinta, T, Lučić, D, Malej, A and Turk, V (2019) Bacteria associated with moon jellyfish during bloom and post-bloom periods in the Gulf of Trieste (northern Adriatic). PLoS ONE 14, e0198056.CrossRefGoogle Scholar
Lee, MD, Kling, JD, Araya, R and Ceh, J (2018) Jellyfish life stages shape associated microbial communities, while a core microbiome is maintained across all. Frontiers in Microbiology 9, 1534.CrossRefGoogle ScholarPubMed
Maas, DL, Prost, S, Bi, K, Smith, LL, Armstrong, EE, Aji, LP, Toha, AHA, Gillespie, RG and Becking, LE (2018) Rapid divergence of mussel populations despite incomplete barriers to dispersal. Molecular Ecology 27, 1556–1571.CrossRefGoogle ScholarPubMed
Mellas, RE, McIlroy, SE, Fitt, WK and Coffroth, MA (2014) Variation in symbiont uptake in the early ontogeny of the upside-down jellyfish, Cassiopea spp. Journal of Experimental Marine Biology and Ecology 459, 38–44.CrossRefGoogle Scholar
Morrow, KM, Moss, AG, Chadwick, NE and Liles, MR (2012) Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Applied and Environmental Microbiology 78, 6438–6449.CrossRefGoogle ScholarPubMed
Neave, MJ, Apprill, A, Ferrier-Pagès, C and Voolstra, CR (2016) Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas. Applied Microbiology and Biotechnology 100, 8315–8324.CrossRefGoogle ScholarPubMed
Neave, MJ, Michell, CT, Apprill, A and Voolstra, CR (2017 a) Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts. Scientific Reports 7, 1–12.CrossRefGoogle ScholarPubMed
Neave, MJ, Rachmawati, R, Xun, L, Michell, CT, Bourne, DG, Apprill, A and Voolstra, CR (2017 b) Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME Journal 11, 186–200.CrossRefGoogle ScholarPubMed
Nei, M and Kumar, S (2000) Molecular Evolution and Phylogenetics. New York, NY: Oxford University Press.Google Scholar
Newkirk, CR, Frazer, TK and Martindale, MQ (2018) Acquisition and proliferation of algal symbionts in bleached polyps of the upside-down jellyfish, Cassiopea xamachana. Journal of Experimental Marine Biology and Ecology 508, 44–51.CrossRefGoogle Scholar
Pitt, KA, Welsh, DT and Condon, RH (2009) Influence of jellyfish blooms on carbon, nitrogen and phosphorus cycling and plankton production. Hydrobiologia 616, 133–149.CrossRefGoogle Scholar
Purba, GY, Haryono, E, Sunarto, S, Manan, J, Rumenta, L, Purwanto, P and Becking, LE (2018) Jellyfish lakes at Misool Islands, Raja Ampat, West Papua, Indonesia. Biodiversitas Journal of Biological Diversity 19, 172–182.CrossRefGoogle Scholar
Quast, C, Pruesse, E, Yilmaz, P, Gerken, J, Schweer, T, Yarza, P, Peplies, J and Glöckner, FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, D590–D596.CrossRefGoogle ScholarPubMed
Shirahama, S and Kakinuma, Y (1985) Differentiation of polyps and influence by Symbiodinium sp. in Mastigias papua. Zoological Society of Japan 2, 931–931.Google Scholar
Shiu, JH and Tang, SL (2019) The bacteria Endozoicomonas: community dynamics, diversity, genomes, and potential impacts on corals. In Li Z (ed.) Symbiotic Microbiomes of Coral Reefs Sponges and Corals. Dordrecht: Springer, pp. 55–67.CrossRefGoogle Scholar
Tamura, K, Peterson, D, Peterson, N, Stecher, G, Nei, M and Kumar, S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Team RC (2013) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. ISBN 3–900051-07-0. Available at http://www.Rproject.orghttp://www.R-project.org.Google Scholar
Tomascik, T and Mah, AJ (1994) The ecology of ‘Halimeda lagoon’: an anchialine lagoon of a raised atoll, Kakaban Island, East Kalimantan, Indonesia. Tropical Biodiversity 2, 385–399.Google Scholar
Urakawa, H, Martens-Habbena, W and Stahl, DA (2010) High abundance of ammonia oxidizing Archaea in coastal waters, determined using a modified DNA extraction method. Applied and Environmental Microbiology 76, 2129–2135.CrossRefGoogle ScholarPubMed
van de Water, JA, Voolstra, CR, Rottier, C, Cocito, S, Peirano, A, Allemand, D and Ferrier-Pagès, C (2018) Seasonal stability in the microbiomes of temperate gorgonians and the red coral Corallium rubrum across the Mediterranean Sea. Microbial Ecology 75, 274–288.CrossRefGoogle ScholarPubMed
Weiland-Bräuer, N, Neulinger, SC, Pinnow, N, Künzel, S, Baines, JF and Schmitz, RA (2015) Composition of bacterial communities associated with Aurelia aurita changes with compartment, life stage, and population. Applied and Environmental Microbiology 81, 6038–6052.CrossRefGoogle ScholarPubMed
Werren, JH, Baldo, L and Clark, ME (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology 6, 741–751.CrossRefGoogle ScholarPubMed
Supplementary material: File

Ferreira et al. supplementary material

Ferreira et al. supplementary material 1

Download Ferreira et al. supplementary material(File)
File 29.7 KB
Supplementary material: File

Ferreira et al. supplementary material

Ferreira et al. supplementary material 2

Download Ferreira et al. supplementary material(File)
File 9.2 KB
Supplementary material: File

Ferreira et al. supplementary material

Ferreira et al. supplementary material 3

Download Ferreira et al. supplementary material(File)
File 100.9 KB
Supplementary material: File

Ferreira et al. supplementary material

Ferreira et al. supplementary material 4

Download Ferreira et al. supplementary material(File)
File 20 KB