Skip to main content

Advertisement

SpringerLink
Log in

Evolutionary relevance of metabolite production in relation to marine sponge bacteria symbiont

  • Applied Microbial and Cell Physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Sponges are habitats for a diverse community of microorganisms. Sponges provide shelter, whereas microbes provide a complementary defensive mechanism. Here, a symbiotic bacterium, identified as Bacillus spp., was isolated from a marine sponge following culture enrichment. Fermentation-assisted metabolomics using thin-layer chromatography (TLC) and gas chromatography-mass spectrometry (GC-MS) indicated that marine simulated nutrition and temperature was the optimum in metabolite production represented by the highest number of metabolites and the diverse chemical classes when compared to other culture media. Following large-scale culture in potato dextrose broth (PDB) and dereplication, compound M1 was isolated and identified as octadecyl-1-(2′,6′-di-tert-butyl-1′-hydroxyphenyl) propionate. M1, at screening concentrations up to 10 mg/ml, showed no activity against prokaryotic bacteria including Staphylococcus aureus and Escherichia coli, while 1 mg/ml of M1 was sufficient to cause a significant killing effect on eukaryotic cells including Candida albicans, Candida auris, and Rhizopus delemar fungi and different mammalian cells. M1 exhibited MIC50 0.97 ± 0.006 and 7.667 ± 0.079 mg/ml against C. albicans and C. auris, respectively. Like fatty acid esters, we hypothesize that M1 is stored in a less harmful form and upon pathogenic attack is hydrolyzed to a more active form as a defensive metabolite. Subsequently, [3-(3,5-di-tert-butyl-4-hydroxyphenyl)-propionic acid] (DTBPA), the hydrolysis product of M1, exhibited ~ 8-fold and 18-fold more antifungal activity than M1 against C. albicans and C. auris, respectively. These findings indicated the selectivity of that compound as a defensive metabolite towards the eukaryotic cells particularly the fungi, a major infectious agent to sponges. Metabolomic-assisted fermentation can provide a significant understanding of a triple marine-evolved interaction.

Key points

• Bacillus species, closely related to uncultured Bacillus, is isolated from Gulf marine sponge

• Metabolomic-assisted fermentations showed diverse metabolites

• An ester with a killing effect against eukaryotes but not prokaryotes is isolated

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The original contributions presented in the study are included in the article and Supplementary Material; further inquiries can be directed to the corresponding author.

References

  • Abad M, Bedoya L, Bermejo (2011) Marin e compounds and their antimicrobial activities. Sci Against Microb Pathog: Commun Curr Res Technol Adv 51:1293–1306

    Google Scholar 

  • Åhman J, Matuschek E, Kahlmeter G (2020) EUCAST evaluation of 21 brands of Mueller-Hinton dehydrated media for disc diffusion testing. CMI 26(10):1412. e1-1412. e5

    PubMed  Google Scholar 

  • Alawad KA, Al-Subhi AM, Alsaafani MA, Alraddadi TM (2023) What causes the Arabian Gulf significant summer sea surface temperature warming trend? Atmosphere 14(3):586

  • Amelia TSM, Suaberon FAC, Vad J, Fahmi ADM, Saludes JP, Bhubalan K (2022) Recent advances of marine sponge-associated microorganisms as a source of commercially viable natural products. Mar Biotechnol 24(3):492–512

    Article  CAS  Google Scholar 

  • Amna T, Amina M, Sharma P, Puri S, Al-Youssef HM, Al-Taweel AM, Qazi G (2012) Effect of precursors feeding and media manipulation on production of novel anticancer pro-drug camptothecin from endophytic fungus. Braz J Microbiol 43(4):1476–1489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arora P, Singh P, Wang Y, Yadav A, Pawar K, Singh A, Padmavati G, Xu J, Chowdhary A (2021) Environmental isolation of Candida auris from the coastal wetlands of Andaman Islands, India. Mbio 12(2):e03181-e3220

    Article  PubMed  PubMed Central  Google Scholar 

  • Ashmawy NS, El-labbad EM, Hamoda AM, El-Keblawy AA, El-Shorbagi A-NA, Mosa KA, Soliman SSM (2022) The anti-Candida activity of Tephrosia apollinea is more superiorly attributed to a novel steroidal compound with selective targeting. Plants 11(16):2120

  • Bachmann E (1990) Ionic balance and osmotic status in carrot (Daucus carota) cell suspensions grown under sodium chloride, osmotic and water stress Plant Nutrition—Physiology and Applications. Springer, pp 495–499

  • Barzkar N, Sohail M, TamadoniJahromi S, Gozari M, Poormozaffar S, Nahavandi R, Hafezieh M (2021) Marine bacterial esterases: emerging biocatalysts for industrial applications. Appl Biochem Biotechnol 193(4):1187–1214

    Article  CAS  PubMed  Google Scholar 

  • Becerro MA, Thacker RW, Turon X, Uriz MJ, Paul VJ (2003) Biogeography of sponge chemical ecology: comparisons of tropical and temperate defenses. Oecologia 135(1):91–101

    Article  PubMed  Google Scholar 

  • Bell JJ (2008) The functional roles of marine sponges. Estuar Coast Shelf Sci 79(3):341–353

    Article  Google Scholar 

  • Benthin S, Villadsen J (1996) Amino acid utilization by Lactococcus lactis subsp. cremoris FD1 during growth on yeast extract or casein peptone. J Appl Microbiol 80(1):65–72

    CAS  Google Scholar 

  • Bills G, Platas G, Fillola A, Jiménez M, Collado J, Vicente F, Martín J, González A, Bur-Zimmermann J, Tormo J (2008) Enhancement of antibiotic and secondary metabolite detection from filamentous fungi by growth on nutritional arrays. J Appl Microbiol 104(6):1644–1658

    Article  CAS  PubMed  Google Scholar 

  • Booth C (1971) Chapter II fungal culture media Methods Microbiol.vol 4. Elsevier, pp 49–94

  • Brinkmann CM, Marker A, Kurtböke DI (2017) An overview on marine sponge-symbiotic bacteria as unexhausted sources for natural product discovery. Diversity 9(4):40

    Article  Google Scholar 

  • Budge SM, Iverson SJ (2003) Quantitative analysis of fatty acid precursors in marine samples: direct conversion of wax ester alcohols and dimethylacetals to FAMEs. J Lipid Res 44(9):1802–1807

    Article  CAS  PubMed  Google Scholar 

  • Calsamiglia S, Stern MD, Firkins J (1995) Effects of protein source on nitrogen metabolism in continuous culture and intestinal digestion in vitro. J Anim Sci 73(6):1819–1827

    Article  CAS  PubMed  Google Scholar 

  • Candau R, Avalos J, Cerda-Olmedo E (1992) Regulation of gibberellin biosynthesis in Gibberella fujikuroi. Plant Physiol 100(3):1184–1188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carballeira NM, Cruz H, Kwong CD, Wan B, Franzblau S (2004) 2-Methoxylated fatty acids in marine sponges: defense mechanism against mycobacteria? Lipids 39(7):675–680

    Article  CAS  PubMed  Google Scholar 

  • Cembella AD (2003) Chemical ecology of eukaryotic microalgae in marine ecosystems. Phycologia 42(4):420–447

    Article  Google Scholar 

  • Cheesbrough M (2005) District laboratory practice in tropical countries, part 2. Cambridge University Press

    Book  Google Scholar 

  • Cortés Y, Hormazábal E, Leal H, Urzúa A, Mutis A, Parra L, Quiroz A (2014) Novel antimicrobial activity of a dichloromethane extract obtained from red seaweed Ceramium rubrum (Hudson)(Rhodophyta: Florideophyceae) against Yersinia ruckeri and Saprolegnia parasitica, agents that cause diseases in salmonids. Electron J Biotechnol 17(3):126–131

    Article  Google Scholar 

  • De Carvalho CC, Fernandes P (2010) Production of metabolites as bacterial responses to the marine environment. Mar Drugs 8(3):705–727

    Article  PubMed  PubMed Central  Google Scholar 

  • Desbois AP, Smith VJ (2010) Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Appl Microbiol Biotechnol 85(6):1629–1642

    Article  CAS  PubMed  Google Scholar 

  • Dintcheva NT, Al-Malaika S, Morici E (2015) Novel organo-modifier for thermally-stable polymer-layered silicate nanocomposites. Polym Degrad Stab 122:88–101

    Article  CAS  Google Scholar 

  • El-Sayed SE, Abdelaziz NA, El-Housseiny GS, Aboshanab KM (2020) Octadecyl 3-(3, 5-di-tert-butyl-4-hydroxyphenyl) propanoate, an antifungal metabolite of Alcaligenes faecalis strain MT332429 optimized through response surface methodology. Appl Microbiol Biotechnol 104(24):10755–10768

    Article  CAS  PubMed  Google Scholar 

  • Engel S, Jensen PR, Fenical W (2002) Chemical ecology of marine microbial defense. J Chem Ecol 28(10):1971–1985

    Article  CAS  PubMed  Google Scholar 

  • Fattorusso E, Gerwick WH, Taglialatela-Scafati O (2012) Handbook of marine natural products. Springer

    Book  Google Scholar 

  • Feng J, Wang F, Liu G, Greenshields D, Shen W, Kaminskyj S, Hughes GR, Peng Y, Selvaraj G, Zou J (2009) Analysis of a Blumeria graminis-secreted lipase reveals the importance of host epicuticular wax components for fungal adhesion and development. Mol Plant Microbe Inter 22(12):1601–1610

    Article  CAS  Google Scholar 

  • Flórez LV, Biedermann PH, Engl T, Kaltenpoth M (2015) Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat Prod Rep 32(7):904–936

    Article  PubMed  Google Scholar 

  • Foti M, Piattelli M, Amico V, Ruberto G (1994) Antioxidant activity of phenolic meroditerpenoids from marine algae. J Photochem Photobiol b: Biol 26(2):159–164

    Article  CAS  Google Scholar 

  • Graça AP, Bondoso J, Gaspar H, Xavier JR, Monteiro MC, de la Cruz M, Oves-Costales D, Vicente F, Lage OM (2013) Antimicrobial activity of heterotrophic bacterial communities from the marine sponge Erylus discophorus (Astrophorida, Geodiidae). PLoS ONE 8(11):e78992

    Article  PubMed  PubMed Central  Google Scholar 

  • Hamdy R, Fayed B, Hamoda AM, Rawas-Qalaji M, Haider M, Soliman SS (2020) Essential oil-based design and development of novel anti-Candida azoles formulation. Molecules (basel, Switzerland) 25(6):1463

    Article  CAS  PubMed  Google Scholar 

  • Harder T, Dobretsov S, Qian P-Y (2004) Waterborne polar macromolecules act as algal antifoulants in the seaweed Ulva reticulata. Mar Ecol Prog Ser 274:133–141

    Article  CAS  Google Scholar 

  • Hug JJ, Krug D, Müller R (2020) Bacteria as genetically programmable producers of bioactive natural products. Nat Rev Chem 4(4):172–193

    Article  CAS  PubMed  Google Scholar 

  • Kabara JJ, Swieczkowski DM, Conley AJ, Truant JP (1972) Fatty acids and derivatives as antimicrobial agents. Antimicrob Agents Chemother 2(1):23–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaiser P, Raina C, Parshad R, Johri S, Verma V, Andrabi KI, Qazi GN (2006) A novel esterase from Bacillus subtilis (RRL 1789): purification and characterization of the enzyme. Protein Expr Purif 45(2):262–268

    Article  CAS  PubMed  Google Scholar 

  • Kim SK, Dewapriya P (2012) Bioactive compounds from marine sponges and their symbiotic microbes: a potential source of nutraceuticals. Adv Food Nutr Res 65:137–151

    Article  PubMed  Google Scholar 

  • Kirkpatrick WR, McAtee RK, Revankar SG, Fothergill AW, McCarthy DI, Rinaldi MG, Patterson TF (1998) Comparative evaluation of national committee for clinical laboratory standards broth macrodilution and agar dilution screening methods for testing fluconazole susceptibility of Cryptococcus neoformans. J Clin Microbiol 36(5):1330–1332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kjelleberg S, Steinberg P, Givskov M, Gram L, Manefield M, de Nys R (1997) Do marine natural products interfere with prokaryotic AHL regulatory systems? Aquat Microb Ecol 13(1):85–93

    Article  Google Scholar 

  • Kubanek J, Jensen PR, Keifer PA, Sullards MC, Collins DO, Fenical W (2003) Seaweed resistance to microbial attack: a targeted chemical defense against marine fungi. PNAS 100(12):6916–6921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lattanzio V, Kroon PA, Quideau S, Treutter D (2009) Plant phenolics—secondary metabolites with diverse functions. Rec Adv Polyphen Res 1:1–35

    Google Scholar 

  • Lopanik NB (2014) Chemical defensive symbioses in the marine environment. Funct Ecol 28(2):328–340

    Article  Google Scholar 

  • Lopanik N, Lindquist N, Targett N (2004) Potent cytotoxins produced by a microbial symbiont protect host larvae from predation. Oecologia 139(1):131–139

    Article  PubMed  Google Scholar 

  • MacWilliams MP, Liao MK (2006) Luria broth (LB) and Luria agar (LA) media and their uses protocol. ASM

  • Mauti GO, Mauti EM, Ouno GA, Shamala FL (2013) Screening of bioactive secondary metabolites from sea sponge (Clathria indica) against bacteria associated with urinary tract infections. Huria: J Open Univ Tanzania 15(1):92–104

    Google Scholar 

  • Miao L, Kwong TF, Qian P-Y (2006) Effect of culture conditions on mycelial growth, antibacterial activity, and metabolite profiles of the marine-derived fungus Arthrinium cf saccharicola. Appl Microbiol Biotechnol 72(5):1063–1073

    Article  CAS  PubMed  Google Scholar 

  • Miki W, Otaki N, Yokoyama A, Kusumi T (1996) Possible origin of zeaxanthin in the marine sponge, Reniera Japonica. Experientia 52(1):93–96

    Article  CAS  Google Scholar 

  • Mondol MAM, Shin HJ, Islam MT (2013) Diversity of secondary metabolites from marine Bacillus species: chemistry and biological activity. Mar Drugs 11(8):2846–2872

    Article  PubMed  PubMed Central  Google Scholar 

  • Najim S, Al-Noor J, Al-Waely W (2015) Extraction of crude peptone from fish wastes for use as a nitrogen source in microbiological media. GJFA 2:29–37

    Google Scholar 

  • Nevenzel JC (1970) Occurrence, function and biosynthesis of wax esters in marine organisms. Lipids 5(3):308–319

    Article  CAS  PubMed  Google Scholar 

  • Perdicaris S, Vlachogianni T, Valavanidis A (2013) Bioactive natural substances from marine sponges: new developments and prospects for future pharmaceuticals. Nat Prod Chem Res 1(3):3–8

    Article  Google Scholar 

  • Richards TA, Jones MD, Leonard G, Bass D (2012) Marine fungi: their ecology and molecular diversity. Annu Rev Mar Sci 4:495–522

    Article  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. Microbiol Res 161(7):604–612

    Article  CAS  Google Scholar 

  • Sargent J (1978) Marine wax esters. Sci Prog Oxf 437–458

  • Sarveswari HB (2020) Marine natural compounds– emerging concepts in bacterial biofilms: Molecular Mechanisms and Control Strategies. p 185

  • Schaller M, Borelli C, Korting HC, Hube B (2005) Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 48(6):365–377

    Article  CAS  PubMed  Google Scholar 

  • Semreen MH, Soliman SSM, Saeed BQ, Alqarihi A, Uppuluri P, Ibrahim AS (2019) Metabolic profiling of Candida auris, a newly-emerging multi-drug resistant Candida species, by GC-MS. Molecules (Basel, Switzerland) 24(3). https://doi.org/10.3390/molecules24030399

  • Shady NH, El-Hossary EM, Fouad MA, Gulder TA, Kamel MS, Abdelmohsen UR (2017) Bioactive natural products of marine sponges from the genus Hyrtios. Molecules (basel, Switzerland) 22(5):781

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith EA, Macfarlane GT (1996) Enumeration of human colonic bacteria producing phenolic and indolic compounds: effects of pH, carbohydrate availability and retention time on dissimilatory aromatic amino acid metabolism. J Appl Bacteriol 81(3):288–302

    Article  CAS  PubMed  Google Scholar 

  • Soliman SS, Tsao R, Raizada MN (2011) Chemical inhibitors suggest endophytic fungal paclitaxel is derived from both mevalonate and non-mevalonate-like pathways. J Nat Prod 74(12):2497–2504. https://doi.org/10.1021/np200303v

    Article  CAS  PubMed  Google Scholar 

  • Soliman S, Alsaadi A, Youssef E, Khitrov G, Noreddin A, Husseiny M, Ibrahim A (2017) Calli essential oils synergize with lawsone against multidrug resistant pathogens. Molecules (basel, Switzerland) 22(12):2223

    Article  PubMed  Google Scholar 

  • Soliman S, Semreen MH, El-Keblawy AA, Abdullah A, Uppuluri P, Ibrahim AS (2017) Assessment of herbal drugs for promising anti-Candida activity. BMC Complement Altern Med 17(1):257. https://doi.org/10.1186/s12906-017-1760-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soliman S, Hamoda AM, El-Shorbagi A-NA, El-Keblawy AA (2019) Novel betulin derivative is responsible for the anticancer folk use of Ziziphus spina-christi from the hot environmental habitat of UAE. J Ethnopharmacol 231:403–408. https://doi.org/10.1016/j.jep.2018.11.040

    Article  CAS  PubMed  Google Scholar 

  • Soliman SSM, Alhamidi TB, Abdin S, Almehdi AM, Semreen MH, Alhumaidi RB, Shakartalla SB, Haider M, Husseiny MI, Omar HA (2020) Effective targeting of breast cancer cells (MCF7) via novel biogenic synthesis of gold nanoparticles using cancer-derived metabolites. PLoS ONE 15(10):e0240156. https://doi.org/10.1371/journal.pone.0240156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stackebrandt E, Goodfellow M (1991) Nucleic acid techniques in bacterial systematics. Wiley

    Google Scholar 

  • Suita SM, Ballester EL, Abreu PC, Wasielesky W Jr (2015) Dextrose as carbon source in the culture of Litopenaeus vannamei (Boone, 1931) in a zero exchange system. Lat Am J Aquat Res 43(3):526–533

    Article  Google Scholar 

  • Suryanarayanan TS (2012) The diversity and importance of fungi associated with marine sponges. Bot Mar 55(6):553–564

    Article  Google Scholar 

  • Sweet M, Bulling M, Cerrano C (2015) A novel sponge disease caused by a consortium of micro-organisms. Coral Reefs 34(3):871–883

    Article  Google Scholar 

  • Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38(7):3022–3027

    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(2):295–347. https://doi.org/10.1128/mmbr.00040-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas TRA, Kavlekar DP, LokaBharathi PA (2010) Marine drugs from sponge-microbe association—a review. Mar Drugs 8(4):1417–1468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tripp HJ, Kitner JB, Schwalbach MS, Dacey JW, Wilhelm LJ, Giovannoni SJ (2008) SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 452(7188):741–744

    Article  CAS  PubMed  Google Scholar 

  • Unson MD, Holland N, 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):1–11

    Article  CAS  Google Scholar 

  • Utkina N, Makarchenko A, Shchelokova O, Virovaya M (2004) Antioxidant activity of phenolic metabolites from marine sponges. Chem Nat Compd 40(4):373–377

    Article  CAS  Google Scholar 

  • VanderMolen KM, Raja HA, El-Elimat T, Oberlies NH (2013) Evaluation of culture media for the production of secondary metabolites in a natural products screening program. AMB Express 3(1):1–7

    Article  CAS  Google Scholar 

  • Vera HD (1948) A simple medium for identification and maintenance of the gonococcus and other bacteria. J Bacteriol 55(4):531–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wakimoto T, Egami Y, Nakashima Y, Wakimoto Y, Mori T, Awakawa T, Ito T, Kenmoku H, Asakawa Y, Piel J (2014) Calyculin biogenesis from a pyrophosphate protoxin produced by a sponge symbiont. Nat Chem Biol 10(8):648–655

    Article  CAS  PubMed  Google Scholar 

  • Webster NS (2007) Sponge disease: a global threat? Environ Microbiol 9(6):1363–1375

    Article  CAS  PubMed  Google Scholar 

  • Yang T, Xiao P, Zhang J, Jia R, Nawaz H, Chen Z, Zhang J (2018) Multifunctional cellulose ester containing hindered phenol groups with free-radical-scavenging and UV-resistant activities. ACS Appl Mater Interfaces 11(4):4302–4310

    Article  Google Scholar 

  • Youcef-Ali M, Chaouche NK, Dehimat L, Bataiche I, Mounira K, Cawoy H, Thonart P (2014) Antifungal activity and bioactive compounds produced by Bacillus mojavensis and Bacillus subtilis. Afr J Microbiol Res 8(6):476–484

    Article  Google Scholar 

  • Yu M, Li Y, Banakar SP, Liu L, Shao C, Li Z, Wang C (2019) New metabolites from the co-culture of marine-derived actinomycete Streptomyces rochei MB037 and fungus Rhinocladiella similis 35. Front Microbiol 10:915

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng CJ, Yoo J-S, Lee T-G, Cho H-Y, Kim Y-H, Kim W-G (2005) Fatty acid synthesis is a target for antibacterial activity of unsaturated fatty acids. FEBS Lett 579(23):5157–5162

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the sampling help provided by Prof. A. Bartholomew, Biology Professor at the American University of Sharjah, UAE.

Funding

This study was funded by the University of Sharjah (grant number 2301110176) to Sameh S. M. Soliman.

Author information

Author notes

  1. Alshaimaa M. Hamoda and Rania Hamdy contributed equally

Authors and Affiliations

  1. Research Institute for Medical and Health Sciences, University of Sharjah, P.O. Box 27272, Sharjah, UAE

    Alshaimaa M. Hamoda, Rania Hamdy, Bahgat Fayed, Ashna Sulaiman, Mohamad Hamad & Sameh S. M. Soliman

  2. College of Medicine, University of Sharjah, P.O. Box 27272, Sharjah, UAE

    Alshaimaa M. Hamoda

  3. Department of Pharmacognosy, Faculty of Pharmacy, Assiut University, Assiut-71526, Egypt

    Alshaimaa M. Hamoda

  4. Faculty of Pharmacy, Zagazig University, Zagazig, Egypt

    Rania Hamdy

  5. Chemistry of Natural and Microbial Product Department, National Research Centre, Cairo, Egypt

    Bahgat Fayed

  6. Department of Biology, Chemistry and Environmental Sciences, College of Arts and Sciences, American University of Sharjah, P.O. Box 26666, Sharjah, UAE

    Mohamed Abouleish

  7. Department of Medical Laboratory Sciences, Collage of Health Sciences, University of Sharjah, P.O. Box 27272, Sharjah, UAE

    Mohamad Hamad

  8. Department of Medicinal Chemistry, College of Pharmacy, University of Sharjah, P.O. Box 27272, Sharjah, UAE

    Sameh S. M. Soliman

Authors
  1. Alshaimaa M. Hamoda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rania Hamdy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bahgat Fayed
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohamed Abouleish
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ashna Sulaiman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mohamad Hamad
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sameh S. M. Soliman
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AH helped in the isolation of sponge-associated bacteria and isolation and characterization of M1, biological activity, and writing the manuscript. RH helped in the rationale design, compound hydrolysis and analysis, cytotoxicity assay, and writing the manuscript. BF helped in bacterial fermentation and media extraction. MA provided the sponge sample and helped in writing the first draft. MH helped in bacterial identification. AS classified the metabolites to different chemical classes. SSMS developed the idea, isolated the bacteria, designed the manuscript, supervised the project, helped in data analysis and interpretation, save the fund, and wrote the manuscript. All authors agree on publishing the data.

Corresponding author

Correspondence to Sameh S. M. Soliman.

Ethics declarations

Ethics approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Consent to participate

Not applicable.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

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

Supplementary information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 468 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hamoda, A.M., Hamdy, R., Fayed, B. et al. Evolutionary relevance of metabolite production in relation to marine sponge bacteria symbiont. Appl Microbiol Biotechnol 107, 5225–5240 (2023). https://doi.org/10.1007/s00253-023-12649-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-023-12649-3

Keywords

Search

Navigation