1887

Abstract

Access to deep-sea sponges brings with it the potential to discover novel antimicrobial candidates, as well as novel cold- and pressure-adapted bacteria with further potential clinical or industrial applications. In this study, we implemented a combination of different growth media, increased pressure and high-throughput techniques to optimize recovery of isolates from two deep-sea hexactinellid sponges, and sp., in the first culture-based microbial analysis of these two sponges. Using 16S rRNA gene sequencing for isolate identification, we found a similar number of cultivable taxa from each sponge species as well as improved recovery of morphotypes from at 22–25 °C compared to other temperatures, which allows a greater potential for screening for novel antimicrobial compounds. Bacteria recovered under conditions of increased pressure were from the phyla , and , except at 4 %O/5 bar, when the phylum was not observed. Cultured isolates from both sponge species displayed antimicrobial activity against and .

Funding
This study was supported by the:
  • Plymouth University (Award NA)
    • Principle Award Recipient: PoppyJ Hesketh-Best
  • Society for Applied Microbiology (Award NA)
    • Principle Award Recipient: MatthewJ Koch
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2021-12-13
2022-01-28
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References

  1. O’Neill J. Tackling Drug-Resistant Infections Globally: Final Report and Recommendations 2016
    [Google Scholar]
  2. Lewis K. New approaches to antimicrobial discovery. Biochem Pharmacol 2017; 134:87–98 [View Article] [PubMed]
    [Google Scholar]
  3. Ling LL, Schneider T, Peoples AJ, Spoering AL, Engels I et al. A new antibiotic kills pathogens without detectable resistance. Nature 2015; 517:455–459 [View Article] [PubMed]
    [Google Scholar]
  4. Love GD, Grosjean E, Stalvies C, Fike DA, Grotzinger JP et al. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 2009; 457:718–721 [View Article] [PubMed]
    [Google Scholar]
  5. Yin Z, Zhu M, Davidson EH, Bottjer DJ, Zhao F et al. Sponge grade body fossil with cellular resolution dating 60 Myr before the Cambrian. Proc Natl Acad Sci U S A 2015; 112:E1453–60 [View Article] [PubMed]
    [Google Scholar]
  6. Weisz JB, Lindquist N, Martens CS. Do associated microbial abundances impact marine demosponge pumping rates and tissue densities?. Oecologia 2008; 155:367–376 [View Article] [PubMed]
    [Google Scholar]
  7. Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR. Marine natural products. Nat Prod Rep 2017; 34:235–294 [View Article] [PubMed]
    [Google Scholar]
  8. Blunt JW, Carroll AR, Copp BR, Davis RA, Keyzers RA et al. Marine natural products. Nat Prod Rep 2018; 35:8–53 [View Article] [PubMed]
    [Google Scholar]
  9. Webster NS, Hill RT. The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by an α-Proteobacterium. Marine Biology 2001; 138:843–851 [View Article]
    [Google Scholar]
  10. Esteves AIS, Hardoim CCP, Xavier JR, Gonçalves JMS, Costa R. Molecular richness and biotechnological potential of bacteria cultured from Irciniidae sponges in the north-east Atlantic. FEMS Microbiol Ecol 2013; 85:519–536 [View Article] [PubMed]
    [Google Scholar]
  11. Montalvo NF, Davis J, Vicente J, Pittiglio R, Ravel J et al. Integration of culture-based and molecular analysis of a complex sponge-associated bacterial community. PLoS One 2014; 9:e90517 [View Article] [PubMed]
    [Google Scholar]
  12. Bergman O, Haber M, Mayzel B, Anderson MA, Shpigel M et al. Marine-based cultivation of diacarnus sponges and the bacterial community composition of wild and maricultured sponges and their larvae. Mar Biotechnol 2011; 13:1169–1182 [View Article]
    [Google Scholar]
  13. Staley JT, Konopka A. Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 1985; 39:321–346 [View Article] [PubMed]
    [Google Scholar]
  14. Henson MW, Lanclos VC, Pitre DM, Weckhorst JL, Lucchesi AM et al. Expanding the diversity of bacterioplankton isolates and modeling isolation efficacy with large-scale dilution-to-extinction cultivation. Appl Environ Microbiol 2020; 86:e00943-20. [View Article] [PubMed]
    [Google Scholar]
  15. Steinert G, Whitfield S, Taylor MW, Thoms C, Schupp PJ. Application of diffusion growth chambers for the cultivation of marine sponge-associated bacteria. Mar Biotechnol 2014; 16:594–603 [View Article]
    [Google Scholar]
  16. Sipkema D, Schippers K, Maalcke WJ, Yang Y, Salim S et al. Multiple approaches to enhance the cultivability of bacteria associated with the marine sponge Haliclona (gellius) sp. Appl Environ Microbiol 2011; 77:2130–2140 [View Article]
    [Google Scholar]
  17. Tamburini C, Canals M, Durrieu de Madron X, Houpert L, Lefèvre D et al. Deep-sea bioluminescence blooms after dense water formation at the ocean surface. PLoS ONE 2013; 8:e67523 [View Article]
    [Google Scholar]
  18. Arístegui J, Gasol JM, Duarte CM, Herndld GJ. Microbial oceanography of the dark ocean’s pelagic realm. Limnol Oceanogr 2009; 54:1501–1529 [View Article]
    [Google Scholar]
  19. Wilkins LGE, Leray M, O’Dea A, Yuen B, Peixoto RS et al. Host-associated microbiomes drive structure and function of marine ecosystems. PLoS Biol 2019; 17:e3000533 [View Article]
    [Google Scholar]
  20. Mangano S, Michaud L, Caruso C, Brilli M, Bruni V et al. Antagonistic interactions between psychrotrophic cultivable bacteria isolated from Antarctic sponges: a preliminary analysis. Research in Microbiology 2009; 160:27–37 [View Article]
    [Google Scholar]
  21. Xin Y, Kanagasabhapathy M, Janussen D, Xue S, Zhang W. Phylogenetic diversity of Gram-positive bacteria cultured from Antarctic deep-sea sponges. Polar Biol 2011; 34:1501–1512 [View Article]
    [Google Scholar]
  22. Steinert G, Busch K, Bayer K, Kodami S, Arbizu PM et al. Compositional and quantitative insights into bacterial and archaeal communities of south pacific deep-sea sponges (Demospongiae and Hexactinellida). Front Microbiol 2020; 11:716 [View Article]
    [Google Scholar]
  23. Bayer K, Busch K, Kenchington E, Beazley L, Franzenburg S et al. Microbial strategies for survival in the glass sponge Vazella pourtalesii. mSystems 2020; 5:e00473-20. [View Article] [PubMed]
    [Google Scholar]
  24. Busch K, Beazley L, Kenchington E, Whoriskey F, Slaby BM et al. Microbial diversity of the glass sponge Vazella pourtalesii in response to anthropogenic activities. Conserv Genet 2020; 21:1001–1010 [View Article]
    [Google Scholar]
  25. Hooper JNA, Van Soest RWM. Systema porifera. A guide to the classification of sponges. In Hooper JNA, Van Soest RWM, Willenz P. eds Systema Porifera Boston, MA: Springer US; 2002 pp 1–7
    [Google Scholar]
  26. Margassery LM, Kennedy J, O’Gara F, Dobson AD, Morrissey JP. Diversity and antibacterial activity of bacteria isolated from the coastal marine sponges Amphilectus fucorum and Eurypon major. Lett Appl Microbiol 2012; 55:2–8 [View Article] [PubMed]
    [Google Scholar]
  27. Kato S, Yamagishi A, Daimon S, Kawasaki K, Tamaki H et al. Isolation of previously uncultured slow-growing bacteria by using a simple modification in the preparation of agar media. Appl Environ Microbiol 2018; 84: [View Article]
    [Google Scholar]
  28. Tagg JR, Bannister LV. “Fingerprinting” beta-haemolytic streptococci by their production of and sensitivity to bacteriocine-like inhibitors. J Med Microbiol 1979; 12:397–411 [View Article] [PubMed]
    [Google Scholar]
  29. Chen Y-L, Lee C-C, Lin Y-L, Yin K-M, Ho C-L et al. Obtaining long 16S rDNA sequences using multiple primers and its application on dioxin-containing samples. BMC Bioinformatics 2015; 16:S13 [View Article]
    [Google Scholar]
  30. Li Y, Zhang L, Xian H, Zhang X. Newly isolated cellulose-degrading bacterium Achromobacter xylosoxidans L2 has deinking potential. BioResources 2019
    [Google Scholar]
  31. Abell GCJ, McOrist AL. Assessment of the diversity and stability of faecal bacteria from healthy adults using molecular methods. Microbial Ecology in Health and Disease 200919229–240 [View Article]
    [Google Scholar]
  32. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991; 173:697–703 [View Article] [PubMed]
    [Google Scholar]
  33. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512–526 [View Article] [PubMed]
    [Google Scholar]
  34. Button DK, Schut F, Quang P, Martin R, Robertson BR. Viability and isolation of marine bacteria by dilution culture: theory, procedures, and initial results. Appl Environ Microbiol 1993; 59:881–891 [View Article]
    [Google Scholar]
  35. Connon SA, Giovannoni SJ. High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new marine isolates. Appl Environ Microbiol 2002; 68:3878–3885 [View Article]
    [Google Scholar]
  36. Edgar RC, Valencia A. Updating the 97% identity threshold for 16S ribosomal RNA OTUs. Bioinformatics 2018; 34:2371–2375 [View Article]
    [Google Scholar]
  37. Young M, Artsatbanov V, Beller HR, Chandra G, Chater KF et al. Genome sequence of the fleming strain of Micrococcus luteus, a simple free-living Actinobacterium. J Bacteriol 2010; 192:841–860 [View Article]
    [Google Scholar]
  38. Slaby BM, Hackl T, Horn H, Bayer K, Hentschel U. Metagenomic binning of a marine sponge microbiome reveals unity in defense but metabolic specialization. ISME J 2017; 11:2465–2478 [View Article]
    [Google Scholar]
  39. Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K et al. Structure and function of the global ocean microbiome. Science 2015; 348:1261359 [View Article]
    [Google Scholar]
  40. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM et al. Microbial diversity in the deep sea and the underexplored “rare biosphere.”. Proceedings of the National Academy of Sciences 2006; 103:12115–12120 [View Article]
    [Google Scholar]
  41. Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C et al. Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun 2016; 7:11870. [View Article] [PubMed]
    [Google Scholar]
  42. Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J 2017; 11:2639–2643 [View Article] [PubMed]
    [Google Scholar]
  43. Cho J-C, Giovannoni SJ. Cultivation and growth characteristics of a diverse group of oligotrophic marine Gammaproteobacteria. Appl Environ Microbiol 2004; 70:432–440 [View Article] [PubMed]
    [Google Scholar]
  44. Zhou M, Dong B, Liu Q. Draft genome sequence of Psychrobacter piscatorii strain LQ58, a psychrotolerant bacterium isolated from a deep-sea hydrothermal vent. Genome Announc 2016; 4:e00044-16. [View Article] [PubMed]
    [Google Scholar]
  45. Oger PM, Jebbar M. The many ways of coping with pressure. Res Microbiol 2010; 161:799–809 [View Article] [PubMed]
    [Google Scholar]
  46. Balansa W, Liu Y, Sharma A, Mihajlovic S et al. Selection of sponge-associated bacteria with high potential for the production of antibacterial compounds. Sci Rep 2020; 10:19614 [View Article] [PubMed]
    [Google Scholar]
  47. Graça AP, Bondoso J, Gaspar H, Xavier JR, Monteiro MC et al. Antimicrobial activity of heterotrophic bacterial communities from the marine sponge Erylus discophorus (Astrophorida, Geodiidae). PLoS One 2013; 8:e78992 [View Article] [PubMed]
    [Google Scholar]
  48. Anteneh YS, Yang Q, Brown MH, Franco CMM. Antimicrobial activities of marine sponge-associated bacteria. Microorganisms 2021; 9:171. [View Article] [PubMed]
    [Google Scholar]
  49. Hamamoto H, Urai M, Ishii K, Yasukawa J, Paudel A et al. Lysocin E is a new antibiotic that targets menaquinone in the bacterial membrane. Nat Chem Biol 2015; 11:127–133 [View Article] [PubMed]
    [Google Scholar]
  50. Bano SA, Naz S, Uzair B, Hussain M, Khan MM et al. Detection of microorganisms with antibacterial activities from different industrial wastes and GC-MS analysis of crude microbial extract. Braz J Biol 2021; 83:e245585 [View Article] [PubMed]
    [Google Scholar]
  51. Deblais L, Rajashekara G. Compound prioritization through meta-analysis enhances the discovery of antimicrobial hits against bacterial pathogens. Antibiotics (Basel) 2021; 10:1065. [View Article] [PubMed]
    [Google Scholar]
  52. Imai Y, Meyer KJ, Iinishi A, Favre-Godal Q, Green R et al. A new antibiotic selectively kills Gram-negative pathogens. Nature 2019; 576:459–464 [View Article] [PubMed]
    [Google Scholar]
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