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Exploring Seaweed-Associated Marine Microbes: Growth Impacts and Enzymatic Potential for Sustainable Resource Utilization

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Abstract

Seaweed, a valuable marine resource widely cultivated worldwide, can be vulnerable to stress and microbiome alterations, resulting in the decay of seaweeds and substantial economic losses. To investigate the seaweed-microbiome interaction, our study aimed to isolate marine bacteria and fungi that can cause Ice–Ice disease and evaluate their enzymatic characteristics for potential application in bioethanol production from seaweed biomass. Three red seaweed species (Gracilaria edulis, Kappaphycus alvarezii, and Eucheuma cottonii) were obtained for our study and placed in separate culture tanks. Among the 18 isolated marine microbial species, 12 tested positive for agar and carrageenan activity: six exhibited both activities, three displayed only agar activity, and three only carrageenan activity. DNA sequencing of the positive microbes identified ten bacteria and two yeast species. The 3,5-Dinitrosalicylic acid (DNSA) assay results revealed that the identified bacterial Caldibacillus kokeshiiformis strain FJAT-47861 exhibited the highest carrageenase activity (0.76 units/ml), while the yeast Pichia fermentans strain PM79 demonstrated the highest agarase activity (0.52 units/ml). Notably, Pichia fermentans strain PM79 exhibited the highest overall agarase and carrageenase activity, averaging 0.63 units/ml. The average carrageenase activity of all six positive microbes was 1.5 times higher than their agarase activity. These findings suggest that the 12 isolated microbes hold potential for bioethanol production from macroalgae, as their agarase and carrageenase activity indicates their ability to break down seaweed cell wall carbohydrates, causing ice–ice disease. Moreover, these results provide exciting prospects for harnessing the bioconversion capabilities of these microbes, paving the way for sustainable and efficient bioethanol production from seaweed resources.

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References

  1. Ali H, Muhammad A, Islam SU, Islam W, Hou Y (2018) A novel bacterial symbiont association in the hispid beetle, Octodonta nipae (Coleoptera: Chrysomelidae), their dynamics and phylogeny. Microb Pathog 118:378–386. https://doi.org/10.1016/j.micpath.2018.03.046

    Article  CAS  PubMed  Google Scholar 

  2. Ali H, Muhammad A, Sanda NB, Huang Y, Hou Y (2019) Pyrosequencing uncovers a shift in bacterial communities across life stages of Octodonta nipae (Coleoptera: Chrysomelidae). Front Microbiol. https://doi.org/10.3389/fmicb.2019.00466

    Article  PubMed  PubMed Central  Google Scholar 

  3. Alsufyani T, Alsufyani T, Califano G, Deicke M, Grueneberg J, Grueneberg J, Weiss A, Weiss A, Engelen AH, Kwantes M, Mohr JF, Mohr JF, Ulrich JF, Wichard T, Wichard T (2020) Macroalgal-bacterial interactions: identification and role of thallusin in morphogenesis of the seaweed Ulva (Chlorophyta). J Exp Bot 71(11):3340–3349. https://doi.org/10.1093/jxb/eraa066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. UshaKiran B, Treasa M, Kaladharan P (2021) Phycocolloid contents in certain economically important seaweeds of Kerala coast, India. J Mar Biol Assoc India 63:05–11. https://doi.org/10.6024/jmbai.2021.63.2.2269-01

    Article  Google Scholar 

  5. Bai MD, Chen CY, Lu WC, Wan HP, Ho SH, Chang JS (2015) Enhancing the oil extraction efficiency of Chlorella vulgaris with cell-disruptive pretreatment using active extracellular substances from Bacillus thuringiensis ITRI-G1. Biochem Eng J 101:185–190. https://doi.org/10.1016/j.bej.2015.05.020

    Article  CAS  Google Scholar 

  6. Burke C, Thomas T, Lewis M, Steinberg P, Kjelleberg S (2011) Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J 5(4):590–600. https://doi.org/10.1038/ismej.2010.164

    Article  CAS  PubMed  Google Scholar 

  7. Cai J, Lovatelli A, Aguilar-Manjarrez J, Cornish L, Dabbadie L, Desrochers A, Diffey S, Garrido Gamarro E, Geehan J, Hurtado A, Lucente D, Mair G, Miao W, Potin P, Przybyla C, Reantaso M, Roubach R, Tauati M, Yuan X (2021) Seaweeds and microalgae: an overview for unlocking their potential in global aquaculture development. FAO Fisheries and Aquaculture Circular No. 1229. Rome, FAO. https://doi.org/10.4060/cb5670en

  8. Califano G, Kwantes M, Abreu MH, Costa R, Wichard T (2020) Cultivating the macroalgal holobiont: effects of integrated multi-trophic aquaculture on the microbiome of Ulva rigida (Chlorophyta). Front Mar Sci. https://doi.org/10.3389/fmars.2020.00052

    Article  Google Scholar 

  9. Campbell AH, Marzinelli EM, Gelber J, Steinberg PD (2015) Spatial variability of microbial assemblages associated with a dominant habitat-forming seaweed. Front Microbiol. https://doi.org/10.3389/fmicb.2015.00230

    Article  PubMed  PubMed Central  Google Scholar 

  10. Coorevits A, Logan NA, Dinsdale AE, Halket G, Scheldeman P, Heyndrickx M, Schumann P, van Landschoot A, de Vos P (2011) Bacillus thermolactis sp. nov., isolated from dairy farms, and emended description of Bacillus thermoamylovorans. Int J Syst Evol Microbiol 61(8):1954–1961. https://doi.org/10.1099/ijs.0.024240-0

    Article  CAS  PubMed  Google Scholar 

  11. Das N, Chandran P (2011) Microbial degradation of petroleum hydrocarbon contaminants: an overview. Biotechnol Res Int 2011:1–13. https://doi.org/10.4061/2011/941810

    Article  CAS  Google Scholar 

  12. Garcıa IG, Pena PJ, Venceslada JB, Martın AM, Santos MM, Gomez ER (2000) Removal of phenol compounds from olive mill wastewater using Phanerochaete chrysosporium, Aspergillus niger, Aspergillus terreus and Geotrichum candidum. Process Biochem 35:751–758

    Article  Google Scholar 

  13. Gerken HG, Donohoe B, Knoshaug EP (2013) Enzymatic cell wall degradation of Chlorella vulgaris and other microalgae for biofuels production. Planta 237(1):239–253. https://doi.org/10.1007/s00425-012-1765-0

    Article  CAS  PubMed  Google Scholar 

  14. Ghaderiardakani F, Coates JC, Wichard T (2017) Bacteria-induced morphogenesis of Ulva intestinalis and Ulva mutabilis (Chlorophyta): a contribution to the lottery theory. FEMS Microbiol Ecol. https://doi.org/10.1093/FEMSEC/FIX094

    Article  PubMed  PubMed Central  Google Scholar 

  15. Gupta RS, Patel S, Saini N, Chen S (2020) Robust demarcation of 17 distinct Bacillus species clades, proposed as novel Bacillaceae genera, by phylogenomics and comparative genomic analyses: description of Robertmurraya kyonggiensis sp. nov. and proposal for an emended genus Bacillus limiting it only to the members of the subtilis and cereus clades of species. Int J Syst Evol Microbiol 70(11):5753–5798. https://doi.org/10.1099/ijsem.0.004475

    Article  CAS  PubMed  Google Scholar 

  16. Ismail A, Ktari L, Ahmed M, Bolhuis H, Boudabbous A, Stal LJ, Cretoiu MS, El Bour M (2016) Antimicrobial activities of bacteria associated with the brown alga Padina pavonica. Front Microbiol. https://doi.org/10.3389/fmicb.2016.01072

    Article  PubMed  PubMed Central  Google Scholar 

  17. Kamilari E, Stanton C, Reen FJ, Ross RP (2023) Uncovering the biotechnological importance of Geotrichum candidum. Foods 12:1124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Khan KA, Al-Ghamdi AA, Ghramh HA, Ansari MJ, Ali H, Alamri SA, Al-Kahtani SN, Adgaba N, Qasim M, Hafeez M (2020) Structural diversity and functional variability of gut microbial communities associated with honey bees. Microb Pathog 138:103793. https://doi.org/10.1016/j.micpath.2019.103793

    Article  PubMed  Google Scholar 

  19. Klinke HB, Thomsen AB, Ahring BK (2004) Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl Microbiol Biotechnol 66:10–26. https://doi.org/10.1007/s00253-004-1642-2

    Article  CAS  PubMed  Google Scholar 

  20. Kong X, Dong R, King T, Chen F, Li H (2022) Biodegradation potential of Bacillus sp. PAH-2 on PAHs for oil-contaminated seawater. Molecules. https://doi.org/10.3390/molecules27030687

    Article  PubMed  PubMed Central  Google Scholar 

  21. Lin G, Sun F, Wang C, Zhang L, Zhang X (2017) Assessment of the effect of Enteromorpha prolifera on bacterial community structures in aquaculture environment. PLoS ONE. https://doi.org/10.1371/journal.pone.0179792

    Article  PubMed  PubMed Central  Google Scholar 

  22. Liu X, Zhao J, Jiang P (2022) Easy removal of epiphytic bacteria on Ulva (Ulvophyceae, Chlorophyta) by vortex with silica sands. Microorganisms. https://doi.org/10.3390/microorganisms10020476

    Article  PubMed  PubMed Central  Google Scholar 

  23. LuizaAstolfi A, Rempel A, Cavanhi VAF, Alves M, Deamici KM, Colla LM, Costa JAV (2020) Simultaneous saccharification and fermentation of Spirulina sp. and corn starch for the production of bioethanol and obtaining biopeptides with high antioxidant activity. Bioresour Technol. https://doi.org/10.1016/j.biortech.2019.122698

    Article  Google Scholar 

  24. Mandree P, Masika W, Naicker J, Moonsamy G, Ramchuran S, Lalloo R (2021) Bioremediation of polycyclic aromatic hydrocarbons from industry contaminated soil using indigenous Bacillus spp. Processes. https://doi.org/10.3390/pr9091606

    Article  Google Scholar 

  25. Matsuo Y, Imagawa H, Nishizawa M, Shizuri Y (2005) Isolation of an algal morphogenesis inducer from a marine bacterium. Science 307(5715):1598. https://doi.org/10.1126/science.1105486

    Article  CAS  PubMed  Google Scholar 

  26. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. J Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030

    Article  CAS  Google Scholar 

  27. Nakanishi K, Nishijima M, Nishimura M, Kuwano K, Saga N (1996) Note bacteria that induce morphogenesis in Ulva pertusa (Chlorophyta) grown under axenic conditions. J Phycol 32:479–482

    Article  Google Scholar 

  28. Offei F, Mensah M, Thygesen A, Kemausuor F (2018) Seaweed bioethanol production: a process selection review on hydrolysis and fermentation. Fermentation. https://doi.org/10.3390/fermentation4040099

    Article  Google Scholar 

  29. Özçimen D, Inan B (2015) An overview of bioethanol production from algae. Biofuels—status and perspective. InTech

    Google Scholar 

  30. Polikovsky M, Califano G, Dunger N, Wichard T, Golberg A (2020) Engineering bacteria-seaweed symbioses for modulating the photosynthate content of Ulva (Chlorophyta): significant for the feedstock of bioethanol production. Algal Res 49:101945. https://doi.org/10.1016/J.ALGAL.2020.101945

    Article  Google Scholar 

  31. Promon SK, Kamal W, Rahman SS, Hossain MM, Choudhury N (2018) Ethanol production using vegetable peels medium and the effective role of cellulolytic bacterial (Bacillus subtilis) pre-treatment. F1000Research. https://doi.org/10.12688/f1000research.13952.1

    Article  PubMed  PubMed Central  Google Scholar 

  32. Rabelo SC, Filho RMI, Costa AC (2009) Lime pretreatment of sugarcane bagasse for bioethanol production. Appl Biochem Biotechnol 153(1–3):139–150. https://doi.org/10.1007/s12010-008-8433-7

    Article  CAS  PubMed  Google Scholar 

  33. Redmond S, Green L, Yarish C, Kim J, Neefus C (2014) New England seaweed culture handbook nursery systems. http://seagrant.uconn.edu

  34. Salehi B, Sharifi-Rad J, Seca AML, Pinto DCGA, Michalak I, Trincone A, Mishra AP, Nigam M, Zam W, Martins N (2019) Current trends on seaweeds: looking at chemical composition, phytopharmacology, and cosmetic applications. Molecules. https://doi.org/10.3390/molecules24224182

    Article  PubMed  PubMed Central  Google Scholar 

  35. Selim KA, El-Ghwas DE, Easa SM, Abdelwahab Hassan MI (2018) Bioethanol a microbial biofuel metabolite; new insights of yeasts metabolic engineering. Fermentation. https://doi.org/10.3390/fermentation4010016

    Article  Google Scholar 

  36. Setyati WA, Susanto AB, Pamungkas DBP, Makrima DB, Senduk JL (2023) Isolation and identification of seaweed-associated bacteria and their antibacterial activity against skin disease agents. Trends Sci. https://doi.org/10.48048/tis.2023.6517

    Article  Google Scholar 

  37. Subramanian M, Maruthamuthu M (2019) Draft genome sequences of two Bacillus spp. and an Oceanobacillus sp. strain isolated from marine macroalgae. Microbiol Resour Announc. https://doi.org/10.1128/mra.01417-18

    Article  PubMed  PubMed Central  Google Scholar 

  38. Sudhakar MP, Kumar BR, Mathimani T, Arunkumar K (2019) A review on bioenergy and bioactive compounds from microalgae and macroalgae-sustainable energy perspective. J Clean Prod 228:1320–1333. https://doi.org/10.1016/j.jclepro.2019.04.287

    Article  CAS  Google Scholar 

  39. Sultana OF, Lee S, Seo H, Mahmud HA, Kim S, Seo A, Kim M, Song HY (2021) Biodegradation and removal of PAHs by Bacillus velezensis isolated from fermented food. J Microbiol Biotechnol 31(7):999–1010. https://doi.org/10.4014/jmb.2104.04023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Tahiluddin AB, Nuñal SN, Luhan MRJ, Santander-De Leon SMS (2021) Vibrio and heterotrophic marine bacteria composition and abundance in nutrient-enriched Kappaphycus striatus. Philipp J Sci 150(6):1751–1763. https://doi.org/10.56899/150.6b.12

    Article  Google Scholar 

  41. Wichard T, Charrier B, Mineur F, Bothwell JH, de Clerck O, Coates JC (2015) The green seaweed Ulva: a model system to study morphogenesis. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00072

    Article  PubMed  PubMed Central  Google Scholar 

  42. Zaynab M, Fatima M, Sharif Y, Zafar MH, Ali H, Khan KA (2019) Role of primary metabolites in plant defense against pathogens. Microbial pathogenesis, vol 137. Academic Press

    Google Scholar 

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Acknowledgements

We thank the seaweed farmers from Rameshwaram, India and specifically Brahma Kamal Research LLP, India for standardizing the seaweed cultivation in the field and providing seaweed samples for this study.

Funding

The authors gratefully acknowledge the Science and Engineering Research Board (SERB), Department of Science and Technology, Government of India (SRG/2022/002212) for their financial assistance.

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  1. Agricultural and Food Engineering Department, Indian Institute of Technology Kharagpur, Kharagpur, West Bengal, 721302, India

    Prakash Saravanan, Antara Chatterjee, K. J. Kiran, Gourav Dhar Bhowmick, Praveen Kumar Sappati & Vishwanath Nagarajan

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Contributions

PS conceptualized and ideated this research under the mentorship of AC and GDB, PS performed the formal analysis and experiments. KKJ and AC assisted in the lab investigations. GDB, PKS, and VN arranged the funding and resources. PS wrote the full original manuscript draft, and GDB did the final edit. All authors read and approved the final manuscript.

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Correspondence to Gourav Dhar Bhowmick.

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Saravanan, P., Chatterjee, A., Kiran, K.J. et al. Exploring Seaweed-Associated Marine Microbes: Growth Impacts and Enzymatic Potential for Sustainable Resource Utilization. Indian J Microbiol (2024). https://doi.org/10.1007/s12088-024-01205-w

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