Bacillus Strains Associated to Homoscleromorpha Sponges are Highly Active Against Multidrug Resistant Bacteria


The search for new, powerful antimicrobials is essential to respond to the current worldwide spread of antibiotic-resistant pathogens. Sponge-associated bacteria have great potential for production of antimicrobials against resistant and multidrug resistant (MDR) pathogenic bacteria, but only few species of the Class Homoscleromorpha have been screened for these activities so far. The aim of this study was to isolate and identify sponge-associated bacteria active against antibiotic-resistant pathogens from sponges of classes Homoscleromorpha and Demospongiae. By employing five different growth conditions, a total of 239 colony-forming units were isolated and remained viable. Among these, 17 (7.1%) isolates presented antimicrobial activity against pathogenic and (multi)drug resistant bacteria including vancomycin-resistant Enterococcus faecalis, Escherichia coli, Citrobacter freundii, Klebsiella penumoniae, Staphylococcus spp. and Streptococcus spp. Bioactive bacteria belonging to genera Bacillus and Vibrio were identified at species level and the DNA fingerprint patterns showed that strains of the same genus were not clonally related. The most active strains belong to genus Bacillus and were isolated from Oscarella sp., Plakina cyanorosea and Chondrilla caribensis. Our results show for the first time that sponge-associated strains of Bacillus pumilus and Bacillus muralis have high anti-MDR activity, and that the Homoscleromorpha may be a better source of such anti-MDR active bacteria than the Demospongiae. These results suggest that marine bacteria associated to homoscleromorph sponges may be an interesting source of new antimicrobial substances with biotechnological potential to treat infections caused by antibiotic-resistant bacteria.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3


  1. 1.

    Ventola CL (2015) The antibiotic resistance crisis: part 1: causes and threats. Pharm Ther 40:277–283

  2. 2.

    Gajdács M (2019) The concept of an ideal antibiotic: implications for drug design. Molecules 24(5):E892.

  3. 3.

    O’Neill J (2014) Antimicrobial resistance: tackling a crisis for the health and wealth of nations. HM Government. Accessed 23 Jan 2019

  4. 4.

    WHO (2014) Antimicrobial resistance: global report on surveillance, pp 1–256. World Health Organization, Geneva. Accessed 23 Jan 2019

  5. 5.

    ECDC/EMEA Joint Technical Report (2009). The bacterial challenge: time to react. European Centre for Disease Prevention and Control; European Medicines Agency, Stockholm. Accessed 23 Jan 2019

  6. 6.

    CDC. Antibiotic/antimicrobial resistance (AR/AMR). Centers for Disease Control and Prevention, Atlanta. Accessed 23 May 2019

  7. 7.

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

  8. 8.

    Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-García C et al (2016) Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun 7:11870.

  9. 9.

    Laport MS (2017) Isolating bacteria from sponges: why and how? Curr Pharm Biotechnol 18:1224–1236.

  10. 10.

    Santos OCS, Pontes PVML, Santos JFM, Muricy G, Giambiagi-de-Marval M, Laport MS (2010) Isolation, characterization and phylogeny of sponge-associated bacteria with antimicrobial activities from Brazil. Res Microbiol 161:604–612.

  11. 11.

    Marinho PR, Moreira AP, Pellegrino FL, Muricy G, Bastos MC, Santos KR, Giambiagi-deMarval M, Laport MS (2009) Marine Pseudomonas putida: a potential source of antimicrobial substances against antibiotic-resistant bacteria. Mem Inst Oswaldo Cruz 104:678–682

  12. 12.

    Santos-Gandelman JF, Giambiagi-deMarval M, Oelemann WMR, Laport MS (2014) Biotechnological potential of sponge-associated bacteria. Curr Pharmac Biotechnol 15:143–155.

  13. 13.

    Laport MS, Bauwens M, de Oliveira NS, Willenz P, George I, Muricy G (2017) Culturable bacterial communities associated to Brazilian Oscarella species (Porifera: Homoscleromorpha) and their antagonistic interactions. Antonie Van Leeuwenhoek 110(4):489–499.

  14. 14.

    de Oliveira BFR, Cavalcanti MD, de Oliveira NS, Lobo LA, Domingues RMCP, Muricy G, Laport MS (2019) Paraclostridium is the main genus of anaerobic bacteria isolated from new species of the marine sponge Plakina in the Brazilian Southeast coast. Curr Microbiol 76:713–722.

  15. 15.

    Rützler K, Duran S, Piantoni C (2007) Adaptation of reef and mangrove sponges to stress: evidence for ecological speciation exemplified by Chondrilla caribensis new species (Demospongiae, Chondrosida). Mar Ecol 28:95–111

  16. 16.

    Muricy G, Domingos C, Lage A, Lanna E, Hardoim C, Laport M, Zilberberg C (2019) Integrative taxonomy widens our knowledge of the diversity, distribution and biology of the genus Plakina (Homosclerophorida: Plakinidae). Invertebr Syst 33:367–401.

  17. 17.

    Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 8(3):268–281.

  18. 18.

    Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504

  19. 19.

    Rodrigues N, Bronzato G, Santiago G, Botelho L, Moreira B, Coelho I, Souza M, Coelho S (2017) The matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) identification versus biochemical tests: a study with enterobacteria from a dairy cattle environment. Braz J Microbiol 48(1):132–138.

  20. 20.

    Laport MS, Santos-Gandelman JF, Muricy G, Giambiagi-deMarval M, George I (2016) Antagonistic interactions among bacteria isolated from either the same or from different sponges native to the Brazilian coast. J Mar Sci Res Dev 6:185.

  21. 21.

    Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703

  22. 22.

    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(21):7188–7196

  23. 23.

    Versalovic J, Schneider M, De Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5:25–40

  24. 24.

    Llor C, Bjerrum L (2014) Antimicrobial resistance: risk associated with antibiotic overuse and initiatives to reduce the problem. Ther Adv Drug Saf 5:229–241

  25. 25.

    Indraningrat AA, Smidt H, Sipkema D (2016) Bioprospecting sponge-associated microbes for antimicrobial compounds. Mar Drugs 14(5):E87.

  26. 26.

    Rane AN, Baikar VV, Ravi Kumar V, Deopurkar RL (2017) Agro-industrial wastes for production of biosurfactant by Bacillus subtilis ANR 88 and its application in synthesis of silver and gold nanoparticles. Front Microbiol 8:492.

  27. 27.

    Pabel CT, Vater J, Wilde C, Franke P, Hofemeister J, Adler B, Bringmann G, Hacker J, Hentschel U (2003) Antimicrobial activities and matrix-assisted laser desorption/ionization mass spectrometry of Bacillus isolates from the marine sponge Aplysina aerophoba. Mar Biotechnol 5:424–434

  28. 28.

    Phelan RW, Barret M, Cotter PD, O’Connor PM, Chen R, Morrissey JP, Dobson ADW, O’Gara F, Barbosa TM (2013) Subtilomycin: a new lantibiotic from Bacillus subtilis Strain MMA7 isolated from the marine Sponge Haliclona simulans. Mar Drugs 11:1878–1898.

  29. 29.

    Suzumura K, Yokoi T, Funatsu M, Nagai K, Tanaka K, Zhang HP, Suzuki K (2003) YM-266183 and YM-266184, novel thiopeptide antibiotics produced by Bacillus cereus isolated from a marine sponge-II Structure elucidation. J Antibiot 56:129–134.

  30. 30.

    Heyrman J, Logan NA, Rodríguez-Díaz M, Scheldeman P, Lebbe L, Swings J, Heyndrickx M, De Vos P (2005) Study of mural painting isolates, leading to the transfer of ‘Bacillus maroccanus’ and ‘Bacillus carotarum’ to Bacillus simplex, emended description of Bacillus simplex, re-examination of the strains previously attributed to ‘Bacillus macroides’ and description of Bacillus muralis sp. nov. Int J Syst Evol Microbiol 55:119–131.

  31. 31.

    WHO (2017) Prioritization of pathogens to guide discovery, research and development of new antibiotics for drug-resistant bacterial infections, including tuberculosis. World Health Organization, Geneva. Accessed 28 June 2018

Download references

Author information

Correspondence to Marinella S. Laport.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 13 kb). Online Resource 1. Specimens of the sponges collected at the coastal shore of the city of Cabo Frio, Rio de Janeiro, SE, Brazil and their associated bacteria viable in five culture media.

Supplementary file2 (XLSX 17 kb). Online Resource 2. Bacteria used as indicator strains in the antimicrobial activity assays.

Supplementary file3 (PDF 424 kb). Online Resource 3. DNA fingerprint patterns in agarose gel electrophoresis obtained by BOX-PCR. (A) Bacillus strains: (1) 43BHI10, (2) 61BHI1, (3) 64BHI2, (4) 84NA4, (5) 84BHI1:105, (6) 64BHI1:101, (7) 64BHI1:1011, (8) 64BHI1:1012, (9) 80BHI3, (10) 80NA7, (11) 80MA4, (12) 80MA7; (B) Vibrio strains: (1) 51BHI25, (2) 51BHI30, (3) 51BHI31, (4) 84BHI6, (5) 84BHI5. The strain and sponge designations correspond to those shown in Table 1.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Freitas-Silva, J., Silva-Oliveira, T., Muricy, G. et al. Bacillus Strains Associated to Homoscleromorpha Sponges are Highly Active Against Multidrug Resistant Bacteria. Curr Microbiol (2020) doi:10.1007/s00284-019-01870-x

Download citation