Bioactivity Screening and Gene-Trait Matching across Marine Sponge-Associated Bacteria
Abstract
:1. Introduction
2. Results
2.1. Genome Characteristics
2.2. Strain Identification and Phylogeny
2.3. Antimicrobial Activity Screening
2.4. Anticancer Activity Screening
2.5. Biosynthetic Gene Cluster Profiling
2.6. Gene-Trait Matching
3. Discussion
4. Materials and Methods
4.1. Isolation of Strains and Growth Conditions
4.2. Strain Identification and Sanger Sequencing
4.3. Chemical Extraction
4.4. Bioactivity Screening Assays
4.4.1. Antimicrobial Activity Test
4.4.2. Cell Viability Assay
4.5. Genomic DNA Extraction and Whole Genome Sequencing
4.6. Bioinformatic Analysis
4.6.1. Quality Control and Genome Assembly
4.6.2. Phylogenetic Analysis and Genome Mining
4.7. Data Visualization and Availability
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Romano, G.; Costantini, M.; Sansone, C.; Lauritano, C.; Ruocco, N.; Ianora, A. Marine microorganisms as a promising and sustainable source of bioactive molecules. Mar. Environ. Res. 2017, 128, 58–69. [Google Scholar] [CrossRef] [PubMed]
- Dyshlovoy, S.A.; Honecker, F. Marine compounds and cancer: The first two decades of XXI century. Mar. Drugs 2019, 18, 20. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Desbois, A.P. How might we increase success in marine-based drug discovery? Expert Opin. Drug Discov. 2014, 9, 985–990. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paterson, I.; Anderson, E.A. The renaissance of natural products as drug candidates. Science 2005, 310, 451–453. [Google Scholar] [CrossRef]
- Marinlit. Available online: http://pubs.rsc.org/marinlit/ (accessed on 20 November 2020).
- Mayer, A.M.; Glaser, K.B.; Cuevas, C.; Jacobs, R.S.; Kem, W.; Little, R.D.; McIntosh, J.M.; Newman, D.J.; Potts, B.C.; Shuster, D.E. The odyssey of marine pharmaceuticals: A current pipeline perspective. Trends Pharmacol. Sci. 2010, 31, 255–265. [Google Scholar] [CrossRef]
- Hu, Y.; Chen, J.; Hu, G.; Yu, J.; Zhu, X.; Lin, Y.; Chen, S.; Yuan, J. Statistical research on the bioactivity of new marine natural products discovered during the 28 years from 1985 to 2012. Mar. Drugs 2015, 13, 202–221. [Google Scholar] [CrossRef]
- Jaspars, M.; De Pascale, D.; Andersen, J.H.; Reyes, F.; Crawford, A.D.; Ianora, A. The marine biodiscovery pipeline and ocean medicines of tomorrow. J. Mar. Biol. 2016, 96, 151–158. [Google Scholar] [CrossRef] [Green Version]
- Hughes, C.C.; Fenical, W. Antibacterials from the sea. Chemistry 2010, 16, 12512–12525. [Google Scholar] [CrossRef] [Green Version]
- Santos, J.D.; Vitorino, I.; Reyes, F.; Vicente, F.; Lage, O.M. From ocean to medicine: Pharmaceutical applications of metabolites from marine bacteria. Antibiotics 2020, 9, 455. [Google Scholar] [CrossRef]
- Pomponi, S.A. The bioprocess-technological potential of the sea. J. Biotechnol. 1999, 70, 5–13. [Google Scholar] [CrossRef]
- Lackner, G.; Peters, E.E.; Helfrich, E.J.; Piel, J. Insights into the lifestyle of uncultured bacterial natural product factories associated with marine sponges. Proc. Natl. Acad. Sci. USA 2017, 114, E347–E356. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sipkema, D.; Franssen, M.C.; Osinga, R.; Tramper, J.; Wijffels, R.H. Marine sponges as pharmacy. Mar. Biotechnol. 2005, 7, 142–162. [Google Scholar] [CrossRef] [PubMed]
- Perdicaris, S.; Vlachoyianni, T.; Valavanidis, A. Bioactive natural substances from marine sponges: New developments and prospects for future pharmaceuticals. Nat. Prod. Chem. Res. 2013, 1, 1–8. [Google Scholar] [CrossRef]
- Paul, V.J.; Puglisi, M.P.; Ritson-Williams, R. Marine chemical ecology. Nat. Prod. Rep. 2006, 23, 153–180. [Google Scholar] [CrossRef] [PubMed]
- Paul, V.J.; Ritson-Williams, R.; Sharp, K. Marine chemical ecology in benthic environments. Nat. Prod. Rep. 2011, 28, 345–387. [Google Scholar] [CrossRef] [PubMed]
- Webster, N.S.; Taylor, M.W. Marine sponges and their microbial symbionts: Love and other relationships. Environ. Microbiol. 2012, 14, 335–346. [Google Scholar] [CrossRef]
- Hentschel, U.; Hopke, J.; Horn, M.; Friedrich, A.B.; Wagner, M.; Hacker, J.; Moore, B.S. Molecular evidence for a uniform microbial community in sponges from different oceans. Appl. Environ. Microbiol. 2002, 68, 4431–4440. [Google Scholar] [CrossRef] [Green Version]
- Pita, L.; Rix, L.; Slaby, B.M.; Franke, A.; Hentschel, U. The sponge holobiont in a changing ocean: From microbes to ecosystems. Microbiome 2018, 6, 46. [Google Scholar] [CrossRef]
- Taylor, M.W.; Radax, R.; Steger, D.; Wagner, M. Sponge-associated microorganisms: Evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 2007, 71, 295–347. [Google Scholar] [CrossRef] [Green Version]
- Thomas, T.; Moitinho-Silva, L.; Lurgi, M.; Bjork, J.R.; Easson, C.; Astudillo-Garcia, C.; Olson, J.B.; Erwin, P.M.; Lopez-Legentil, S.; Luter, H.; et al. Diversity, structure and convergent evolution of the global sponge microbiome. Nat. Commun. 2016, 7, 11870. [Google Scholar] [CrossRef] [Green Version]
- Piel, J. Metabolites from symbiotic bacteria. Nat. Prod. Rep. 2009, 26, 338–362. [Google Scholar] [CrossRef] [PubMed]
- Wilson, M.C.; Mori, T.; Ruckert, C.; Uria, A.R.; Helf, M.J.; Takada, K.; Gernert, C.; Steffens, U.A.; Heycke, N.; Schmitt, S.; et al. An environmental bacterial taxon with a large and distinct metabolic repertoire. Nature 2014, 506, 58–62. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Morita, M.; Schmidt, E.W. Parallel lives of symbionts and hosts: Chemical mutualism in marine animals. Nat. Prod. Rep. 2018, 35, 357–378. [Google Scholar] [CrossRef] [PubMed]
- Tianero, M.D.; Balaich, J.N.; Donia, M.S. Localized production of defence chemicals by intracellular symbionts of Haliclona sponges. Nat. Microbiol. 2019, 4, 1149–1159. [Google Scholar] [CrossRef] [PubMed]
- Piel, J.; Hui, D.; Wen, G.; Butzke, D.; Platzer, M.; Fusetani, N.; Matsunaga, S. Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei. Proc. Natl. Acad. Sci. USA 2004, 101, 16222–16227. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Santos-Gandelman, J.F.; Giambiagi-deMarval, M.; Oelemann, W.M.; Laport, M.S. Biotechnological potential of sponge-associated bacteria. Curr. Pharm. Biotechnol. 2014, 15, 143–155. [Google Scholar] [CrossRef] [PubMed]
- Gomes, N.G.; Dasari, R.; Chandra, S.; Kiss, R.; Kornienko, A. Marine invertebrate metabolites with anticancer activities: Solutions to the “supply problem”. Mar. Drugs 2016, 14, 98. [Google Scholar] [CrossRef]
- Moore, B.S. Biosynthesis of marine natural products: Macroorganisms (part b). Nat. Prod. Rep. 2006, 23, 615–629. [Google Scholar] [CrossRef]
- Waters, A.L.; Peraud, O.; Kasanah, N.; Sims, J.W.; Kothalawala, N.; Anderson, M.A.; Abbas, S.H.; Rao, K.V.; Jupally, V.R.; Kelly, M.; et al. An analysis of the sponge Acanthostrongylophora igens’ microbiome yields an actinomycete that produces the natural product manzamine A. Front. Mar. Sci. 2014, 1, 54. [Google Scholar] [CrossRef] [Green Version]
- Moitinho-Silva, L.; Nielsen, S.; Amir, A.; Gonzalez, A.; Ackermann, G.L.; Cerrano, C.; Astudillo-Garcia, C.; Easson, C.; Sipkema, D.; Liu, F.; et al. The sponge microbiome project. Gigascience 2017, 6, 1–7. [Google Scholar] [CrossRef]
- Thomas, T.R.; Kavlekar, D.P.; LokaBharathi, P.A. Marine drugs from sponge-microbe association—A review. Mar. Drugs 2010, 8, 1417–1468. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mehbub, M.F.; Lei, J.; Franco, C.; Zhang, W. Marine sponge derived natural products between 2001 and 2010: Trends and opportunities for discovery of bioactives. Mar. Drugs 2014, 12, 4539–4577. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Indraningrat, A.A.; Smidt, H.; Sipkema, D. Bioprospecting sponge-associated microbes for antimicrobial compounds. Mar. Drugs 2016, 14, 87. [Google Scholar] [CrossRef] [PubMed]
- Brinkmann, C.M.; Marker, A.; Kurtböke, D.I. An overview on marine sponge-symbiotic bacteria as unexhausted sources for natural product discovery. Diversity 2017, 9, 40. [Google Scholar] [CrossRef] [Green Version]
- Kiran, G.S.; Priyadharsini, S.; Sajayan, A.; Ravindran, A.; Selvin, J. An antibiotic agent pyrrolo[1,2-a]pyrazine-1,4-dione,hexahydro isolated from a marine bacteria Bacillus tequilensis MSI45 effectively controls multi-drug resistant Staphylococcus aureus. RSC Adv. 2018, 8, 17837–17846. [Google Scholar] [CrossRef] [Green Version]
- Cao, D.D.; Trinh, T.T.V.; Mai, H.D.T.; Vu, V.N.; Le, H.M.; Thi, Q.V.; Nguyen, M.A.; Duong, T.T.; Tran, D.T.; Chau, V.M.; et al. Antimicrobial lavandulylated flavonoids from a sponge-derived Streptomyces sp. G248 in East Vietnam Sea. Mar. Drugs 2019, 17, 529. [Google Scholar] [CrossRef] [Green Version]
- Ibrahim, A.H.; Attia, E.Z.; Hajjar, D.; Anany, M.A.; Desoukey, S.Y.; Fouad, M.A.; Kamel, M.S.; Wajant, H.; Gulder, T.A.M.; Abdelmohsen, U.R. New cytotoxic cyclic peptide from the marine sponge-associated Nocardiopsis sp. UR67. Mar. Drugs 2018, 16, 290. [Google Scholar] [CrossRef] [Green Version]
- Karanam, G.; Arumugam, M.K.; Sirpu Natesh, N. Anticancer effect of marine sponge-associated Bacillus pumilus AMK1 derived dipeptide cyclo (-pro-tyr) in human liver cancer cell line through apoptosis and G2/M phase arrest. Int. J. Pept. Res. Ther. 2019, 26, 445–457. [Google Scholar] [CrossRef]
- Lindequist, U. Marine-derived pharmaceuticals-challenges and opportunities. Biomol. Ther. 2016, 24, 561–571. [Google Scholar] [CrossRef] [Green Version]
- Reen, F.J.; Romano, S.; Dobson, A.D.; O’Gara, F. The sound of silence: Activating silent biosynthetic gene clusters in marine microorganisms. Mar. Drugs 2015, 13, 4754–4783. [Google Scholar] [CrossRef] [Green Version]
- Zhang, G.; Li, J.; Zhu, T.; Gu, Q.; Li, D. Advanced tools in marine natural drug discovery. Curr. Opin. Biotechnol. 2016, 42, 13–23. [Google Scholar] [CrossRef] [PubMed]
- Bachmann, B.O.; Van Lanen, S.G.; Baltz, R.H. Microbial genome mining for accelerated natural products discovery: Is a renaissance in the making? J. Ind. Microbiol. 2014, 41, 175–184. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Versluis, D.; Nijsse, B.; Naim, M.A.; Koehorst, J.J.; Wiese, J.; Imhoff, J.F.; Schaap, P.J.; van Passel, M.W.J.; Smidt, H.; Sipkema, D. Comparative genomics highlights symbiotic capacities and high metabolic flexibility of the marine genus Pseudovibrio. Genome Biol. Evol. 2018, 10, 125–142. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Versluis, D.; McPherson, K.; van Passel, M.W.J.; Smidt, H.; Sipkema, D. Recovery of previously uncultured bacterial genera from three mediterranean sponges. Mar. Biotechnol. 2017, 19, 454–468. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- NCBI nr/nt Database. Available online: https://www.ncbi.nlm.nih.gov/ (accessed on 20 November 2020).
- Genome Taxonomy Database (GTDB). Available online: https://gtdb.ecogenomic.org/ (accessed on 20 November 2020).
- Parks, D.H.; Chuvochina, M.; Chaumeil, P.A.; Rinke, C.; Mussig, A.J.; Hugenholtz, P. A complete domain-to-species taxonomy for bacteria and archaea. Nat. Biotechnol. 2020, 38, 1079–1086. [Google Scholar] [CrossRef] [PubMed]
- Blin, K.; Shaw, S.; Steinke, K.; Villebro, R.; Ziemert, N.; Lee, S.Y.; Medema, M.H.; Weber, T. AntiSMASH 5.0: Updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res. 2019, 47, W81–W87. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Blin, K.; Shaw, S.; Kautsar, S.A.; Medema, M.H.; Weber, T. The antiSMASH database version 3: Increased taxonomic coverage and new query features for modular enzymes. Nucleic Acids Res. 2021, 49, D639–D643. [Google Scholar] [CrossRef]
- Kokoulin, M.S.; Kuzmich, A.S.; Romanenko, L.A.; Chikalovets, I.V.; Chernikov, O.V. Structure and in vitro bioactivity against cancer cells of the capsular polysaccharide from the marine bacterium Psychrobacter marincola. Mar. Drugs 2020, 18, 268. [Google Scholar] [CrossRef]
- Yin, H.; Guo, C.; Wang, Y.; Liu, D.; Lv, Y.; Lv, F.; Lu, Z. Fengycin inhibits the growth of the human lung cancer cell line 95D through reactive oxygen species production and mitochondria-dependent apoptosis. Anticancer Drugs 2013, 24, 587–598. [Google Scholar] [CrossRef]
- Ma, Z.; Wang, N.; Hu, J.; Wang, S. Isolation and characterization of a new iturinic lipopeptide, mojavensin A produced by a marine-derived bacterium Bacillus mojavensis B0621A. J. Antibiot. 2012, 65, 317–322. [Google Scholar] [CrossRef] [Green Version]
- Chuyen, H.V.; Eun, J.B. Marine carotenoids: Bioactivities and potential benefits to human health. Crit. Rev. Food Sci. Nutr. 2017, 57, 2600–2610. [Google Scholar] [CrossRef] [PubMed]
- Galasso, C.; Corinaldesi, C.; Sansone, C. Carotenoids from marine organisms: Biological functions and industrial applications. Antioxidants 2017, 6, 96. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sheikhpour, M.; Sadeghi, A.; Yazdian, F.; Movafagh, A.; Mansoori, A. Anticancer and apoptotic effects of ectoine and hydroxyectoine on non-small cell lung cancer cells: An in-vitro investigation. Multidiscip. Cancer Investig. 2019, 3, 14–19. [Google Scholar] [CrossRef] [Green Version]
- Kalinovskaya, N.I.; Romanenko, L.A.; Irisawa, T.; Ermakova, S.P.; Kalinovsky, A.I. Marine isolate Citricoccus sp. KMM 3890 as a source of a cyclic siderophore nocardamine with antitumor activity. Microbiol. Res. 2011, 166, 654–661. [Google Scholar] [CrossRef] [PubMed]
- Gutleben, J.; Chaib De Mares, M.; van Elsas, J.D.; Smidt, H.; Overmann, J.; Sipkema, D. The multi-omics promise in context: From sequence to microbial isolate. Crit. Rev. Microbiol. 2017, 44, 212–229. [Google Scholar] [CrossRef] [Green Version]
- Lee, L.H.; Goh, B.H.; Chan, K.G. Editorial: Actinobacteria: Prolific producers of bioactive metabolites. Front. Microbiol. 2020, 11, 1612. [Google Scholar] [CrossRef]
- Brinkmann, C.; Kearns, P.; Evans-Illidge, E.; Kurtböke, D. Diversity and bioactivity of marine bacteria associated with the sponges Candidaspongia flabellata and Rhopaloeides odorabile from the Great Barrier Reef in Australia. Diversity 2017, 9, 39. [Google Scholar] [CrossRef] [Green Version]
- Desriac, F.; Jegou, C.; Balnois, E.; Brillet, B.; Le Chevalier, P.; Fleury, Y. Antimicrobial peptides from marine proteobacteria. Mar. Drugs 2013, 11, 3632–3660. [Google Scholar] [CrossRef] [Green Version]
- Khalifa, S.A.M.; Elias, N.; Farag, M.A.; Chen, L.; Saeed, A.; Hegazy, M.F.; Moustafa, M.S.; Abd El-Wahed, A.; Al-Mousawi, S.M.; Musharraf, S.G.; et al. Marine natural products: A source of novel anticancer drugs. Mar. Drugs 2019, 17, 491. [Google Scholar] [CrossRef] [Green Version]
- Graca, A.P.; Bondoso, J.; Gaspar, H.; Xavier, J.R.; Monteiro, M.C.; de la Cruz, M.; Oves-Costales, D.; Vicente, F.; Lage, O.M. Antimicrobial activity of heterotrophic bacterial communities from the marine sponge Erylus discophorus (Astrophorida, Geodiidae). PLoS ONE 2013, 8, e78992. [Google Scholar] [CrossRef] [Green Version]
- Chelossi, E.; Milanese, M.; Milano, A.; Pronzato, R.; Riccardi, G. Characterisation and antimicrobial activity of epibiotic bacteria from Petrosia ficiformis (Porifera, Demospongiae). J. Exp. Mar. Biol. Ecol. 2004, 309, 21–33. [Google Scholar] [CrossRef]
- Abdelmohsen, U.R.; Bayer, K.; Hentschel, U. Diversity, abundance and natural products of marine sponge-associated actinomycetes. Nat. Prod. Rep. 2014, 31, 381–399. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Zhao, Z.; Wang, H. Cytotoxic natural products from marine sponge-derived microorganisms. Mar. Drugs 2017, 15, 68. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Calcabrini, C.; Catanzaro, E.; Bishayee, A.; Turrini, E.; Fimognari, C. Marine sponge natural products with anticancer potential: An updated review. Mar. Drugs 2017, 15, 310. [Google Scholar] [CrossRef] [Green Version]
- Cetkovic, H.; Halasz, M.; Herak Bosnar, M. Sponges: A reservoir of genes implicated in human cancer. Mar. Drugs 2018, 16, 20. [Google Scholar] [CrossRef] [Green Version]
- Romano, S. Ecology and biotechnological potential of bacteria belonging to the genus Pseudovibrio. Appl. Environ. Microbiol. 2018, 84, e02516-17. [Google Scholar] [CrossRef] [Green Version]
- Rodrigues, A.M.S.; Rohée, C.; Fabre, T.; Batailler, N.; Sautel, F.; Carletti, I.; Nogues, S.; Suzuki, M.T.; Stien, D. Cytotoxic indole alkaloids from Pseudovibrio denitrificans BBCC725. Tetrahedron Lett. 2017, 58, 3172–3173. [Google Scholar] [CrossRef] [Green Version]
- Choi, E.J.; Kwon, H.C.; Ham, J.; Yang, H.O. 6-Hydroxymethyl-1-phenazine-carboxamide and 1,6-phenazinedimethanol from a marine bacterium, Brevibacterium sp. KMD 003, associated with marine purple vase sponge. J. Antibiot. 2009, 62, 621–624. [Google Scholar] [CrossRef]
- Guerrero-Garzón, J.F.; Zehl, M.; Schneider, O.; Rückert, C.; Busche, T.; Kalinowski, J.; Bredholt, H.; Zotchev, S.B. Streptomyces spp. from the marine sponge Antho dichotoma: Analyses of secondary metabolite biosynthesis gene clusters and some of their products. Front. Microbiol. 2020, 11, 437. [Google Scholar] [CrossRef] [Green Version]
- Naughton, L.M.; Romano, S.; O’Gara, F.; Dobson, A.D.W. Identification of secondary metabolite gene clusters in the Pseudovibrio genus reveals encouraging biosynthetic potential toward the production of novel bioactive compounds. Front. Microbiol. 2017, 8, 1494. [Google Scholar] [CrossRef] [Green Version]
- Xu, L.; Ye, K.X.; Dai, W.H.; Sun, C.; Xu, L.H.; Han, B.N. Comparative genomic insights into secondary metabolism biosynthetic gene cluster distributions of marine Streptomyces. Mar. Drugs 2019, 17, 498. [Google Scholar] [CrossRef] [Green Version]
- Ceniceros, A.; Dijkhuizen, L.; Petrusma, M.; Medema, M.H. Genome-based exploration of the specialized metabolic capacities of the genus Rhodococcus. BMC Genomics 2017, 18, 593. [Google Scholar] [CrossRef] [PubMed]
- Doroghazi, J.R.; Metcalf, W.W. Comparative genomics of actinomycetes with a focus on natural product biosynthetic genes. BMC Genomics 2013, 14, 611. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thompson, D.; Cognat, V.; Goodfellow, M.; Koechler, S.; Heintz, D.; Carapito, C.; Van Dorsselaer, A.; Mahmoud, H.; Sangal, V.; Ismail, W. Phylogenomic classification and biosynthetic potential of the fossil fuel-biodesulfurizing Rhodococcus strain IGTS8. Front. Microbiol. 2020, 11, 1417. [Google Scholar] [CrossRef] [PubMed]
- Behnsen, J.; Raffatellu, M. Siderophores: More than stealing iron. mBio 2016, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schneider, Y.; Jenssen, M.; Isaksson, J.; Hansen, K.O.; Andersen, J.H.; Hansen, E.H. Bioactivity of serratiochelin A, a siderophore isolated from a co-culture of Serratia sp. and Shewanella sp. Microorganisms 2020, 8, 1042. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Zhou, H.; Chen, H.; Jing, X.; Zheng, W.; Li, R.; Sun, T.; Liu, J.; Fu, J.; Huo, L.; et al. Discovery of recombinases enables genome mining of cryptic biosynthetic gene clusters in Burkholderiales species. Proc. Natl. Acad. Sci. USA 2018, 115, E4255–E4263. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luo, S.; Chen, X.A.; Mao, X.M.; Li, Y.Q. Regulatory and biosynthetic effects of the bkd gene clusters on the production of daptomycin and its analogs A21978C1-3. J. Ind. Microbiol. 2018, 45, 271–279. [Google Scholar] [CrossRef]
- Kanafani, Z.A.; Corey, G.R. Daptomycin: A rapidly bactericidal lipopeptide for the treatment of gram-positive infections. Expert Rev. Anti-Infect. Ther. 2007, 5, 177–184. [Google Scholar] [CrossRef]
- Roch, M.; Gagetti, P.; Davis, J.; Ceriana, P.; Errecalde, L.; Corso, A.; Rosato, A.E. Daptomycin resistance in clinical MRSA strains is associated with a high biological fitness cost. Front. Microbiol. 2017, 8, 2303. [Google Scholar] [CrossRef] [Green Version]
- Cheng, W.; Feng, Y.Q.; Ren, J.; Jing, D.; Wang, C. Anti-tumor role of Bacillus subtilis fmbj-derived fengycin on human colon cancer HT29 cell line. Neoplasma 2016, 63, 215–222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sivapathasekaran, C.; Das, P.; Mukherjee, S.; Saravanakumar, J.; Mandal, M.; Sen, R. Marine bacterium derived lipopeptides: Characterization and cytotoxic activity against cancer cell lines. Int. J. Pept. Res. Ther. 2010, 16, 215–222. [Google Scholar] [CrossRef]
- Krubasik, P.; Sandmann, G. A carotenogenic gene cluster from Brevibacterium linens with novel lycopene cyclase genes involved in the synthesis of aromatic carotenoids. Mol. Gen. Genet. 2000, 263, 423–432. [Google Scholar] [CrossRef] [PubMed]
- Kearney, S.E.; Zahoranszky-Kohalmi, G.; Brimacombe, K.R.; Henderson, M.J.; Lynch, C.; Zhao, T.; Wan, K.K.; Itkin, Z.; Dillon, C.; Shen, M.; et al. Canvass: A crowd-sourced, natural-product screening library for exploring biological space. ACS Cent. Sci. 2018, 4, 1727–1741. [Google Scholar] [CrossRef]
- Lane, D.J. 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematic; Stackebrandt, E., Goodfellow, M., Eds.; John Wiley and Sons: New York, NY, USA, 1991. [Google Scholar]
- Gavriilidou, A.; Gutleben, J.; Versluis, D.; Forgiarini, F.; van Passel, M.W.J.; Ingham, C.J.; Smidt, H.; Sipkema, D. Comparative genomic analysis of Flavobacteriaceae: Insights into carbohydrate metabolism, gliding motility and secondary metabolite biosynthesis. BMC Genomics 2020, 21, 569. [Google Scholar] [CrossRef]
- Hall, T. BioEdit: An important software for molecular biology. GERF Bull. Biosci. 2011, 2, 60–61. [Google Scholar]
- Altschul, S.F.; Gish, W.; Miller, W.; Myers, E.W.; Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215, 403–410. [Google Scholar] [CrossRef]
- Monteiro, M.C.; de la Cruz, M.; Cantizani, J.; Moreno, C.; Tormo, J.R.; Mellado, E.; De Lucas, J.R.; Asensio, F.; Valiante, V.; Brakhage, A.A.; et al. A new approach to drug discovery: High-throughput screening of microbial natural extracts against Aspergillus fumigatus using resazurin. J. Biomol. Screen 2012, 17, 542–549. [Google Scholar] [CrossRef]
- Martin, J.; Sousa, D.S.; Crespo, G.; Palomo, S.; Gonzalez, I.; Tormo, J.R.; de la Cruz, M.; Anderson, M.; Hill, R.T.; Vicente, F.; et al. Kocurin, the true structure of PM181104, an anti-methicillin-resistant Staphylococcus aureus (MRSA) thiazolyl peptide from the marine-derived bacterium Kocuria palustris. Mar. Drugs 2013, 11, 387–398. [Google Scholar] [CrossRef] [Green Version]
- Santos, J.D.; Vitorino, I.; de la Cruz, M.; Díaz, C.; Cautain, B.; Annang, F.; Pérez-Moreno, G.; Gonzalez, I.; Tormo, J.R.; Martin, J.; et al. Diketopiperazines and other bioactive compounds from bacterial symbionts of marine sponges. Antonie Leeuwenhoek 2020, 113, 875–887. [Google Scholar] [CrossRef]
- Audoin, C.; Bonhomme, D.; Ivanisevic, J.; de la Cruz, M.; Cautain, B.; Monteiro, M.C.; Reyes, F.; Rios, L.; Perez, T.; Thomas, O.P. Balibalosides, an original family of glucosylated sesterterpenes produced by the mediterranean sponge Oscarella balibaloi. Mar. Drugs 2013, 11, 1477–1489. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Andrews, S. FastQC: A Quality Control Tool for High Throughput Sequence Data. 2010. Available online: http://www.bioinformatics.babraham.ac.uk/projects/fastqc (accessed on 20 November 2020).
- Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A flexible trimmer for illumina sequence data. Bioinformatics 2014, 30, 2114–2120. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bankevich, A.; Nurk, S.; Antipov, D.; Gurevich, A.A.; Dvorkin, M.; Kulikov, A.S.; Lesin, V.M.; Nikolenko, S.I.; Pham, S.; Prjibelski, A.D.; et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 2012, 19, 455–477. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bushnell, B.; Rood, J.; Singer, E. BBMerge—Accurate paired shotgun read merging via overlap. PLoS ONE 2017, 12, e0185056. [Google Scholar] [CrossRef] [PubMed]
- Langmead, B.; Salzberg, S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 2012, 9, 357–359. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, H.; Handsaker, B.; Wysoker, A.; Fennell, T.; Ruan, J.; Homer, N.; Marth, G.; Abecasis, G.; Durbin, R.; 1000 Genome Project Data Processing Subgroup. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25, 2078–2079. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Quinlan, A.R. Bedtools: The swiss-army tool for genome feature analysis. Curr. Protoc. Bioinform. 2014, 47, 11.12.11–11.12.34. [Google Scholar] [CrossRef] [PubMed]
- Gurevich, A.; Saveliev, V.; Vyahhi, N.; Tesler, G. QUAST: Quality assessment tool for genome assemblies. Bioinformatics 2013, 29, 1072–1075. [Google Scholar] [CrossRef] [PubMed]
- Parks, D.H.; Imelfort, M.; Skennerton, C.T.; Hugenholtz, P.; Tyson, G.W. CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015, 25, 1043–1055. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chaumeil, P.A.; Mussig, A.J.; Hugenholtz, P.; Parks, D.H. GTDB-Tk: A toolkit to classify genomes with the genome taxonomy database. Bioinformatics 2020, 36, 1925–1927. [Google Scholar] [CrossRef] [PubMed]
- Parks, D.H.; Chuvochina, M.; Waite, D.W.; Rinke, C.; Skarshewski, A.; Chaumeil, P.A.; Hugenholtz, P. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 2018, 36, 996–1004. [Google Scholar] [CrossRef] [PubMed]
- Price, M.N.; Dehal, P.S.; Arkin, A.P. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS ONE 2010, 5, e9490. [Google Scholar] [CrossRef] [PubMed]
- Letunic, I.; Bork, P. Interactive tree of life (iTOL) v3: An online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 2016, 44, W242–W245. [Google Scholar] [CrossRef] [PubMed]
- R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2018; Available online: https://www.R-project.org/ (accessed on 20 November 2020).
- Wickham, H. ggplot2: Elegant Graphics for Data Analysis; Springer: New York, NY, USA, 2016. [Google Scholar]
Strain ID | Isolation Source | Best BLAST hit | ID% | Genome Size (Mbp) | GC Content (%) | Total Gene Count |
---|---|---|---|---|---|---|
Aa3_DN55_6A7 | Aplysina aerophoba | Bradyrhizobium sp. | 100 | 7.2 | 64.6 | 6655 |
Pf1_Ps_8H04_1 1 | Petrosia ficiformis | Pseudovibrio sp. | 99.9 | 5.7 | 48.2 | 5174 |
Pf1_DN206_4B7 1 | Petrosia ficiformis | Pseudovibrio sp. | 99.85 | 5.1 | 52.8 | 4692 |
Irc_Ps_AB108 1 | Ircinia sp. | Pseudovibrio sp. | 100 | 5.9 | 44.6 | 5369 |
Pf1_DN64_8G1 | Petrosia ficiformis | Pseudovibrio sp. | 99.93 | 5.8 | 51.4 | 5275 |
Aa3_DN64_1D3 1 | Aplysina aerophoba | Pseudovibrio sp. | 99.93 | 5.8 | 50.3 | 5239 |
Pf1_Ps_8H06 1 | Petrosia ficiformis | Pseudovibrio sp. | 100 | 6.1 | 49.7 | 5554 |
Cn_Ps_AB111 1 | Chondrilla nucula | Pseudovibrio sp. | 99.89 | 5.9 | 49.8 | 5423 |
Aa3_Str.68_7G12 1 | Aplysina aerophoba | Pseudovibrio sp. | 100 | 5.9 | 51.0 | 5288 |
Acac_Ps_AB113 1 | Acanthella acuta | Pseudovibrio sp. | 99.93 | 5.4 | 51.0 | 4886 |
Aa3_DN166_3E9_2 | Aplysina aerophoba | Ruegeria sp. | 99.93 | 4.6 | 56.2 | 4558 |
Pf1_DN81_6F7_2 | Petrosia ficiformis | Ruegeria atlantica | 100 | 4.5 | 57.9 | 4356 |
Cc1_DN217_4H2 | Corticium candelabrum | Microbulbifer echini | 99.85 | 4.7 | 49.8 | 4229 |
Aa3_DN138_5C8 | Aplysina aerophoba | Acinetobacter radioresistens | 100 | 3.3 | 41.4 | 3085 |
Pf1_DN14_7A9_1 | Petrosia ficiformis | Psychrobacter celer | 100 | 2.9 | 46.8 | 2434 |
Aa3_DN73_5E10 | Aplysina aerophoba | Psychrobacter celer | 100 | 2.6 | 47.0 | 2194 |
Aa3_DN30_1H2 | Aplysina aerophoba | Aquimarina macrocephali | 100 | 5.4 | 32.9 | 4684 |
Aa3_DN216_4B10_1 | Aplysina aerophoba | Rhodococcus erythropolis | 100 | 7.1 | 62.5 | 6770 |
Aa3_DN213_3F7 | Aplysina aerophoba | Brevibacterium aurantiacum | 100 | 4.2 | 63.0 | 3850 |
Aa3_DN216_4B10_2 | Aplysina aerophoba | Janibacter melonis | 99.93 | 3.4 | 72.9 | 3220 |
Aa3_DN71_7G3_2 | Aplysina aerophoba | Bacillus frigoritolerans | 100 | 4.9 | 40.5 | 4807 |
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Gavriilidou, A.; Mackenzie, T.A.; Sánchez, P.; Tormo, J.R.; Ingham, C.; Smidt, H.; Sipkema, D. Bioactivity Screening and Gene-Trait Matching across Marine Sponge-Associated Bacteria. Mar. Drugs 2021, 19, 75. https://doi.org/10.3390/md19020075
Gavriilidou A, Mackenzie TA, Sánchez P, Tormo JR, Ingham C, Smidt H, Sipkema D. Bioactivity Screening and Gene-Trait Matching across Marine Sponge-Associated Bacteria. Marine Drugs. 2021; 19(2):75. https://doi.org/10.3390/md19020075
Chicago/Turabian StyleGavriilidou, Asimenia, Thomas Andrew Mackenzie, Pilar Sánchez, José Ruben Tormo, Colin Ingham, Hauke Smidt, and Detmer Sipkema. 2021. "Bioactivity Screening and Gene-Trait Matching across Marine Sponge-Associated Bacteria" Marine Drugs 19, no. 2: 75. https://doi.org/10.3390/md19020075