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Antimicrobial activity and diversity of bacteria associated with Taiwanese marine sponge Theonella swinhoei

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Abstract

Marine sponges often rely on other epiphytes for protection from harmful predators. To understand the diversity and antimicrobial activity present among epiphytic bacteria isolated from marine sponge. We used both the 16S rRNA tag pyrosequencing method and the culture-based method to investigate the bacterial communities of Theonella swinhoei collected off the shore of southern Taiwan. Eight-hundred and eighteen operational taxonomic units (OTUs; 97% sequence similarity) were identified from 23,700 sponge-derived sequence tags. The bacteria associated with T. swinhoei were found to be highly diverse—as many as 12 different phyla of bacteria were identified. However, in terms of population evenness, the community was dominated by two phyla—Acidobacteria (71.54%) and Chloroflexi (19.60%). A total of 700 bacterial strains were isolated and cultured from samples of the sponge T. swinhoei. Within these culturable strains, only 12% were Actinomycetes. Despite the low percentage of Actinobacteria from the samples, among the 51 strains of culturable bacteria that showed high antimicrobial activity, a great majority (62%) were Actinomycetes (30 strains of Streptomyces and 1 strain each of Micromonospora and Brevibacterium). The remaining isolates that produced antimicrobial compounds were Gammaproteobacteria (10 strains of Pseudoalteromonas) and Firmicutes (8 and 1 strains of Bacillus and Paenibacillus, respectively). We speculated that many more Actinomycetes are yet to be isolated from T. swinhoei microbiota. Advanced techniques, such as high-throughput culture and culturome, should allow the isolation and purification of these medically important groups of bacteria from sponge.

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References

  • Abdelmohsen UR, Bayer K, Hentschel U (2014) Diversity, abundance and natural products of marine sponge-associated actinomycetes. Nat Prod Rep 31:381–399

    Article  CAS  PubMed  Google Scholar 

  • Barns SM, Cain EC, Sommerville L, Kuske CR (2007) Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol 73:3113–3116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bayer K, Schmitt S, Hentschel U (2008) Physiology, phylogeny and in situ evidence for bacterial and archaeal nitrifiers in the marine sponge Aplysina aerophoba. Environ Microbiol 10:2942–2955

    Article  CAS  PubMed  Google Scholar 

  • Bengtsson MM, Ovreas L (2010) Planctomycetes dominate biofilms on surfaces of the kelp Laminaria hyperborea. BMC Microbiol 10:261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bewley CA, Holland ND, Faulkner DJ (1996) Two classes of metabolites from Theonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia 52:716–722

    Article  CAS  PubMed  Google Scholar 

  • Bredholdt H, Galatenko OA, Engelhardt K, Fjaervik E, Terekhova LP, Zotchev SB (2007) Rare actinomycete bacteria from the shallow water sediments of the Trondheim fjord, Norway: isolation, diversity and biological activity. Environ Microbiol 9:2756–2764

    Article  CAS  PubMed  Google Scholar 

  • Breuker A, Koweker G, Blazejak A, Schippers A (2011) The deep biosphere in terrestrial sediments in the Chesapeake bay area, Virginia, USA. Front Microbiol 2:156

    Article  PubMed  PubMed Central  Google Scholar 

  • Burgess JG, Jordan EM, Bregu M, Mearns-Spragg A, Boyd KG (1999) Microbial antagonism: a neglected avenue of natural products research. J Biotechnol 70:27–32

    Article  CAS  PubMed  Google Scholar 

  • Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardenas CA, Bell JJ, Davy SK, Hoggard M, Taylor MW (2014) Influence of environmental variation on symbiotic bacterial communities of two temperate sponges. FEMS Microbiol Ecol 88:516–527

    Article  CAS  PubMed  Google Scholar 

  • Chen Y-H, Kuo J, Sung P-J et al (2012) Isolation of marine bacteria with antimicrobial activities from cultured and field-collected soft corals. World J Microbiol Biotechnol 28:3269–3279

    Article  CAS  PubMed  Google Scholar 

  • Chen Y-H, Lu M-C, Chung H-M et al (2016) Bafilomycin M, a new cytotoxic bafilomycin produced by a Streptomyces sp. isolated from a marine sponge Theonella sp. Tetrahedron Lett 57:4863–4865

    Article  CAS  Google Scholar 

  • Closek CJ, Sunagawa S, DeSalvo MK et al (2014) Coral transcriptome and bacterial community profiles reveal distinct Yellow Band Disease states in Orbicella faveolata. ISME J 8:2411–2422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cole JR, Chai B, Farris RJ et al (2005) The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 33:D294–D296

    Article  CAS  PubMed  Google Scholar 

  • Flatt PM, Gautschi JT, Thacker RW, Musafija-Girt M, Crews P, Gerwick WH (2005) Identification of the cellular site of polychlorinated peptide biosynthesis in the marine sponge Dysidea (Lamellodysidea) herbacea and symbiotic cyanobacterium Oscillatoria spongeliae by CARD-FISH analysis. Mar Biol 147:761–774

    Article  CAS  Google Scholar 

  • Flemer B, Kennedy J, Margassery LM, Morrissey JP, O’Gara F, Dobson AD (2012) Diversity and antimicrobial activities of microbes from two Irish marine sponges, Suberites carnosus and Leucosolenia sp. J Appl Microbiol 112:289–301

    Article  CAS  PubMed  Google Scholar 

  • Gerwick WH, Moore BS (2012) Lessons from the past and charting the future of marine natural products drug discovery and chemical biology. Biol Chem 19:85–98

    Article  CAS  Google Scholar 

  • Graca AP, Bondoso J, Gaspar H et al (2013) Antimicrobial activity of heterotrophic bacterial communities from the marine sponge Erylus discophorus (Astrophorida, Geodiidae). PLoS One 8:e78992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hardoim CC, Costa R (2014) Temporal dynamics of prokaryotic communities in the marine sponge Sarcotragus spinosulus. Mol Ecol 23:3097–3112

    Article  CAS  PubMed  Google Scholar 

  • Hentschel U, Schmid M, Wagner M, Fieseler L, Gernert C, Hacker J (2001) Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS Microbiol Ecol 35:305–312

    Article  CAS  PubMed  Google Scholar 

  • Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J, Moore BS (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68:4431–4440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill M, Hill A, Lopez N, Harriott O (2006) Sponge-specific bacterial symbionts in the Caribbean sponge, Chondrilla nucula (Demospongiae, Chondrosida). Mar Biol 148:1221–1230

    Article  Google Scholar 

  • Hoffmann F, Radax R, Woebken D et al (2009) Complex nitrogen cycling in the sponge Geodia barretti. Environ Microbiol 11:2228–2243

    Article  CAS  PubMed  Google Scholar 

  • Ivanitskaia LP, Singal EM, Bibikova MV, Vostrov SN (1978) Directed isolation of Micromonospora generic cultures on a selective medium with gentamycin. Antibiotiki 23:690–692

    CAS  PubMed  Google Scholar 

  • Jensen PR, Gontang E, Mafnas C, Mincer TJ, Fenical W (2005) Culturable marine actinomycete diversity from tropical Pacific Ocean sediments. Environ Microbiol 7:1039–1048

    Article  PubMed  Google Scholar 

  • Jetten MS (2008) The microbial nitrogen cycle. Environ Microbiol 10:2903–2909

    Article  CAS  PubMed  Google Scholar 

  • Jin L, Liu F, Sun W, Zhang F, Karuppiah V, Li Z (2014) Pezizomycotina dominates the fungal communities of South China Sea sponges Theonella swinhoei and Xestospongia testudinaria. FEMS Microbiol Ecol 90:935–945

    Article  CAS  PubMed  Google Scholar 

  • Kellogg CA, Ross SW, Brooke SD (2016) Bacterial community diversity of the deep-sea octocoral Paramuricea placomus. PeerJ 4:e2529

    Article  PubMed  PubMed Central  Google Scholar 

  • Kennedy J, Baker P, Piper C et al (2009) Isolation and analysis of bacteria with antimicrobial activities from the marine sponge Haliclona simulans collected from Irish waters. Mar Biotechnol 11:384–396

    Article  CAS  Google Scholar 

  • Keren R, Lavy A, Mayzel B, Ilan M (2015) Culturable associated-bacteria of the sponge Theonella swinhoei show tolerance to high arsenic concentrations. Front Microbiol 6:154

    Article  PubMed  PubMed Central  Google Scholar 

  • Kindaichi T, Yuri S, Ozaki N, Ohashi A (2012) Ecophysiological role and function of uncultured Chloroflexi in an anammox reactor. Water Sci Technol 66:2556–2561

    Article  CAS  PubMed  Google Scholar 

  • Kiss H, Nett M, Domin N et al (2011) Complete genome sequence of the filamentous gliding predatory bacterium Herpetosiphon aurantiacus type strain (114-95(T)). Stand Genomic Sci 5:356–370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lavy A, Keren R, Haber M, Schwartz I, Ilan M (2014) Implementing sponge physiological and genomic information to enhance the diversity of its culturable associated bacteria. FEMS Microbiol Ecol 87:486–502

    Article  CAS  PubMed  Google Scholar 

  • Leal MC, Puga J, Serodio J, Gomes NC, Calado R (2012) Trends in the discovery of new marine natural products from invertebrates over the last two decades—where and what are we bioprospecting? PLoS One 7:e30580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin CH, Chuang CH, Twan WH et al (2016) Seasonal changes in bacterial communities associated with healthy and diseased Porites coral in southern Taiwan. Can J Microbiol 62:1021–1033

    Article  CAS  PubMed  Google Scholar 

  • Lu M-C, Du Y-C, Chuu J-J et al (2009) Active extracts of wild fruiting bodies of Antrodia camphorata (EEAC) induce leukemia HL 60 cells apoptosis partially through histone hypoacetylation and synergistically promote anticancer effect of trichostatin A. Arch Toxicol 83:121–129

    Article  CAS  PubMed  Google Scholar 

  • Mehbub MF, Lei J, Franco C, Zhang W (2014) Marine sponge derived natural products between 2001 and 2010: trends and opportunities for discovery of bioactives. Mar Drugs 12:4539–4577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohamed NM, Saito K, Tal Y, Hill RT (2010) Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J 4:38–48

  • Montalvo NF, Davis J, Vicente J, Pittiglio R, Ravel J, Hill RT (2014) Integration of culture-based and molecular analysis of a complex sponge-associated bacterial community. PLoS One 9:e90517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ng JC, Chan Y, Tun HM, Leung FC, Shin PK, Chiu JM (2015) Pyrosequencing of the bacteria associated with Platygyra carnosus corals with skeletal growth anomalies reveals differences in bacterial community composition in apparently healthy and diseased tissues. Front Microbiol 6:1142

    PubMed  PubMed Central  Google Scholar 

  • Nithyanand P, Manju S, Karutha Pandian S (2011) Phylogenetic characterization of culturable actinomycetes associated with the mucus of the coral Acropora digitifera from Gulf of Mannar. FEMS Microbiol Lett 314:112–118

    Article  CAS  PubMed  Google Scholar 

  • O’Connor-Sanchez A, Rivera-Dominguez AJ, Santos-Briones Cde L, Lopez-Aguiar LK, Pena-Ramirez YJ, Prieto-Davo A (2014) Acidobacteria appear to dominate the microbiome of two sympatric Caribbean sponges and one Zoanthid. Biol Res 47:67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osinga R, Armstrong E, Grant Burgess J, Hoffmann F, Reitner J, Schumann-Kindel G (2001) Sponge–microbe associations and their importance for sponge bioprocess engineering. Hydrobiologia 461:55–62

    Article  Google Scholar 

  • Piel J, Hui D, Wen G, Butzke D, Platzer M, Fusetani N, Matsunaga S (2004) Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei. Proc Natl Acad Sci U S A 101:16222–16227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pimentel-Elardo S, Wehrl M, Friedrich AB, Jensen PR, Hentschel U (2003) Isolation of planctomycetes from Aplysina sponges. Aquat Microb Ecol 33:239–245

    Article  Google Scholar 

  • Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reveillaud J, Maignien L, Eren AM, Huber JA, Apprill A, Sogin ML, Vanreusel A (2014) Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J 8:1198–1209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-R LM, Konstantinidis KT (2014) Nonpareil: a redundancy-based approach to assess the level of coverage in metagenomic datasets. Bioinformatics 30:629–635

    Article  CAS  PubMed  Google Scholar 

  • Santos OC, Pontes PV, Santos JF, Muricy G, Giambiagi-deMarval M, Laport MS (2010) Isolation, characterization and phylogeny of sponge-associated bacteria with antimicrobial activities from Brazil. Res Microbiol 161:604–612

    Article  CAS  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75

  • Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt EW, Obraztsova AY, Davidson SK, Faulkner DJ, Haygood MG (2000) Identification of the antifungal peptide-containing symbiont of the marine sponge Theonella swinhoei as a novel δ-proteobacterium, “Candidatus Entotheonella palauensis”. Mar Biol 136:969–977

    Article  CAS  Google Scholar 

  • Schmitt S, Deines P, Behnam F, Wagner M, Taylor MW (2011) Chloroflexi bacteria are more diverse, abundant, and similar in high than in low microbial abundance sponges. FEMS Microbiol Ecol 78:497–510

    Article  CAS  PubMed  Google Scholar 

  • Schmitt S, Hentschel U, Taylor MW (2012) Deep sequencing reveals diversity and community structure of complex microbiota in five Mediterranean sponges. Hydrobiologia 687:341–351

    Article  CAS  Google Scholar 

  • Simister R, Taylor MW, Tsai P, Fan L, Bruxner TJ, Crowe ML, Webster N (2012) Thermal stress responses in the bacterial biosphere of the Great Barrier Reef sponge, Rhopaloeides odorabile. Environ Microbiol 14:3232–3246

    Article  CAS  PubMed  Google Scholar 

  • Simister R, Taylor MW, Rogers KM, Schupp PJ, Deines P (2013) Temporal molecular and isotopic analysis of active bacterial communities in two New Zealand sponges. FEMS Microbiol Ecol 85:195–205

    Article  PubMed  Google Scholar 

  • Stern NJ, Svetoch EA, Eruslanov BV et al (2006) Isolation of a Lactobacillus salivarius strain and purification of its bacteriocin, which is inhibitory to Campylobacter jejuni in the chicken gastrointestinal system. Antimicrob Agents Chemother 50:3111–3116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terekhova LP, Galatenko OA, Alferova IV, Preobragenskaya TP (1991) Comparative estimation of some bacterial growth inhibitors as selective agents for isolation of soil actinomycetes. Antibiot Chemother 36:5–8

    CAS  Google Scholar 

  • Thomas TRA, Kavlekar DP, LokaBharathi PA (2010) Marine drugs from sponge-microbe association—a review. Mar Drugs 8:1417–1468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thoms C, Horn M, Wagner M, Hentschel U, Proksch P (2003) Monitoring microbial diversity and natural product profiles of the sponge Aplysina cavernicola following transplantation. Mar Biol 142:685–692

    Article  CAS  Google Scholar 

  • Unson MD, Faulkner DJ (1993) Cyanobacterial symbiont biosynthesis of chlorinated metabolites from Dysidea herbacea (Porifera). Experientia 49:349–353

    Article  CAS  Google Scholar 

  • Unson MD, Holland ND, Faulkner DJ (1994) A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue. Mar Biol 119:1–11

    Article  CAS  Google Scholar 

  • Ward NL, Challacombe JF, Janssen PH et al (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webster NS, Hill RT (2001) The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by an alpha-proteobacterium. Mar Biol 138:843–851

  • Webster NS, Taylor MW (2012) Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol 14:335–346

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson CR, Fay P (1979) Nitrogen fixation in coral reef sponges with symbiotic cyanobacteria. Nature 279:527–529

    Article  CAS  Google Scholar 

  • Wilkinson CR, Nowak M, Austin B, Colwell RR (1981) Specificity of bacterial symbionts in Mediterranean and Great Barrier Reef sponges. Microb Ecol 7:13–21

    Article  CAS  PubMed  Google Scholar 

  • Wilson GS, Raftos DA, Corrigan SL, Nair SV (2010) Diversity and antimicrobial activities of surface-attached marine bacteria from Sydney Harbour, Australia. Microbiol Res 165:300–311

    Article  CAS  PubMed  Google Scholar 

  • Ye Q, Wu Y, Zhu Z, Wang X, Li Z, Zhang J (2016) Bacterial diversity in the surface sediments of the hypoxic zone near the Changjiang Estuary and in the East China Sea. MicrobiologyOpen 5:323–339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Li Z, Miao X, Zhang F (2009) The screening of antimicrobial bacteria with diverse novel nonribosomal peptide synthetase (NRPS) genes from South China Sea sponges. Mar Biotechnol 11:346–355

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by intramural funding from the National Museum of Marine Biology and Aquarium.

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Authors and Affiliations

  1. Department of Planning and Research, National Museum of Marine Biology and Aquarium, Pingtung, 944, Taiwan

    Jimmy Kuo, Mei-Chin Lu & Ping-Jung Sung

  2. Graduate Institute of Marine Biology, National Dong Hwa University, Pingtung, 944, Taiwan

    Jimmy Kuo, Yu-Ting Yang, Mei-Chin Lu & Ping-Jung Sung

  3. Department of Biological Sciences, University of Memphis, Memphis, TN, 38152, USA

    Tit-Yee Wong

  4. Department of Life Sciences, National University of Kaohsiung, Kaohsiung, 811, Taiwan

    Yung-Sen Huang

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Taxonomy assignments of the bacterial community associated with marine sponge Theonella swinhoei at different levels. (XLSX 53.9 kb)

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Kuo, J., Yang, YT., Lu, MC. et al. Antimicrobial activity and diversity of bacteria associated with Taiwanese marine sponge Theonella swinhoei. Ann Microbiol 69, 253–265 (2019). https://doi.org/10.1007/s13213-018-1414-3

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