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Cite this paper: |
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Rediat ABATE, Buce Hanoch HETHARUA, Vishal PATIL, Daner LIN, Demeke KIFLE, Junrong LIANG, Changping CHEN, Lin SUN, Shuh-Ji KAO, Yonghong BI, Bangqin HUANG, Yahui GAO. Responses of phytoplankton and its satellite bacteria to exogenous ethanol[J]. Journal of Oceanology and Limnology, 2023, 41(1): 203-214 |
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Responses of phytoplankton and its satellite bacteria to exogenous ethanol |
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| Rediat ABATE1,2,3, Buce Hanoch HETHARUA4, Vishal PATIL2, Daner LIN2, Demeke KIFLE5, Junrong LIANG2,3, Changping CHEN2,3, Lin SUN2,4, Shuh-Ji KAO4, Yonghong BI1, Bangqin HUANG3,4, Yahui GAO2,3,4 |
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1 Key Laboratory of Algal Biology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China;
2 School of Life Sciences, Xiamen University, Xiamen 361102, China;
3 Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystem, College of Environment&Ecology, Xiamen University, Xiamen 361102, China;
4 State Key Laboratory of Marine Environmental Sciences, Xiamen University, Xiamen 361101, China;
5 Department of Zoological Sciences, Addis Ababa University, Addis Ababa, PO Box 1176, Ethiopia |
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| Abstract: |
| The response of phytoplankton and its satellite bacteria to various concentrations (0.01%–10% v/v) of ethanol is studied. To elucidate the effect of ethanol, single-strains of phytoplankton (SSP) culture, pure strains of satellite bacteria isolated from nonaxenic SSP cultures, and Escherichia coli were screened. Results indicate that ethanol could promote the growth and photosynthetic efficiency (Fv/Fm) of SSP at 0.01% and the growth of satellite bacteria at 0.01%–1%. Nevertheless, ethanol inhibited the growth and Fv/Fm of SSP at 0.1%–1%, and killed bacteria and SSP at 10% concentration. Further investigation on a satellite bacterium (Mameliella alba) revealed that ethanol promotes growth by serving as a growth stimulant rather than a metabolic carbon source. The 16S rRNA gene amplicon indicated that all nonaxenic SSP cultures harbor distinct satellite bacteria communities where the SSP culture of Skeletonema costatum, Phaeodactylum tricornutum, and Dunaliella bardawil were dominated by bacteria genera of Marivita (~80%), Dinoroseobacter (~47%), and Halomonas (~87%), respectively, indicating that every SSP cultures have their own distinct satellite bacterial community. The bacteria family Rhodobacteraceae was dominant in the two marine diatoms, whereas Halomonadaceae was dominant in the saline green microalga. Compared to their respective controls, the supply of 0.5% ethanol to SSP cultures promoted the growth of the satellite bacteria but did not cause a significant difference in species composition of satellite bacteria. Therefore, a low concentration of ethanol can promote the growth of bacteria in a non-selective way. This study enriched our knowledge about the effect of ethanol on aquatic microbes and provided a baseline for basic and applied biotechnological research in the aquatic environment in the future. |
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| Key words:
aquatic microbes|bacteria diversity|ethanol effect|growth inhibition|growth stimulation
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| Received: 2021-07-13 Revised: |
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References:
Azam F, Malfatti F. 2007. Microbial structuring of marine ecosystems. Nature Reviews Microbiology, 5(10): 782-791.
Bezerra R P, Matsudo M C, Pérez Mora L S et al. 2014.Ethanol effect on batch and fed-batch Arthrospira platensis growth. Journal of Industrial Microbiology & Biotechnology, 41(4): 687-692.
Chatterjee I, Somerville G A, Heilmann C et al. 2006. Very low ethanol concentrations affect the viability and growth recovery in post-stationary-phase Staphylococcus aureus populations. Applied and Environmental Microbiology, 72(4): 2627-2636.
Chen A I, Dolben E F, Okegbe C et al. 2014. Candida albicans ethanol stimulates Pseudomonas aeruginosa WspR-controlled biofilm formation as part of a cyclic relationship involving phenazines. PLoS Pathogens, 10(10): e1004480.
Clark D P, Cronan J E. 2005. Two-carbon compounds and fatty acids as carbon sources. EcoSal Plus, 1(2): 1-34, https://doi.org/10.1128/ecosalplus.3.4.4.
Cole J J. 1982. Interactions between bacteria and algae in aquatic ecosystems. Annual Review of Ecology and Systematics, 13: 291-314.
Crocker A W, Harty C E, Hammond J H et al. 2019.Pseudomonas aeruginosa ethanol oxidation by AdhA in low-oxygen environments. Journal of Bacteriology, 201(23): e00393-19.
El Jay A. 1996. Toxic effects of organic solvents on the growth of Chlorella vulgaris and Selenastrum capricornutum.Bulletin of Environmental Contamination and Toxicology, 57(2): 191-198.
Feris K, Mackay D, de Sieyes N et al. 2008. Effect of ethanol on microbial community structure and function during natural attenuation of benzene, toluene, and o-xylene in a sulfate-reducing aquifer. Environmental Science & Technology, 42(7): 2289-2294.
Ferraro C M, Finkel S E. 2019. Physiological, genetic, and transcriptomic analysis of alcohol-induced delay of Escherichia coli death. Applied and Environmental Microbiology, 85(2): e02113-18.
Field C B, Behrenfeld M J, Randerson J T et al. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science, 281(5374): 237-240.
Fujita T, Aoyagi H, Ogbonna J C et al. 2008. Effect of mixed organic substrate on α-tocopherol production by Euglena gracilis in photoheterotrophic culture. Applied Microbiology and Biotechnology, 79(3): 371-378.
Fukui K, Kato K, Kodama T et al. 1988. ATP formation in aerobic catabolism of ethanol by oral Streptococci. Proceedings of the Japan Academy, Series B, 64(1): 13-16.
Ghosh M, Anthony C, Harlos K et al. 1995. The refined structure of the quinoprotein methanol dehydrogenase from Methylobacterium extorquens at 1.94 å. Structure, 3(2):177-187, https://doi.org/10.1016/S0969-2126(01)00148-4.
Guillard R R L, Ryther J H. 1962. Studies of marine planktonic diatoms: I. Cyclotella nana Husted, and Detonula confervacea (Cleve) Gran. Canadian Journal of Microbiology, 8(2): 229-239.
Guillard R R L, Sieracki M S. 2005. Counting cells in cultures with the light microscope. In: Andersen R A ed . Algal Culturing Techniques . Elsevier Academic Press , London .p. 239-252.
He P J, Han W H, Shao L M et al. 2018. One-step production of C6-C8 carboxylates by mixed culture solely grown on CO. Biotechnology for Biofuels, 11(1): 4.
Hetharua B, Min D R, Liao H et al. 2018. Litorivita pollutaquae gen. nov., sp. nov., a marine bacterium in the family Rhodobacteraceae isolated from surface seawater of Xiamen Port, China. International Journal of Systematic and Evolutionary Microbiology, 68(12): 3908-3913.
Huo S H, Kong M, Zhu F F et al. 2018. Mixotrophic Chlorella sp. UJ-3 cultivation in the typical anaerobic fermentation effluents. Bioresource Technology, 249: 219-225.
Ingram L O N, Buttke T M. 1985. Effects of alcohols on microorganisms. Advances in Microbial Physiology, 25: 253-300.
Ingram L O. 1981. Mechanism of lysis of Escherichia coli by ethanol and other chaotropic agents. Journal of Bacteriology, 146(1): 331-336.
Jasti S, Sieracki M E, Poulton N J et al. 2005. Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton. Applied and Environmental Microbiology, 71(7): 3483-3494.
Jones T H, Vail K M, McMullen L M. 2013. Filament formation by foodborne bacteria under sublethal stress. International Journal of Food Microbiology, 165(2): 97-110.
Kato S, Kitamura E, Yamamoto S et al. 1991. Effects of sodium chloride, ethanol, glucose content and pH on the growth of lactic acid bacteria isolated from salted “Daikon”(Raphanus sativus). Nippon Shokuhin Kogyo Gakkaishi, 38(10): 962-966.
Kawarai T, Wachi M, Ogino H et al. 2004. SulA-independent filamentation of Escherichia coli during growth after release from high hydrostatic pressure treatment. Applied Microbiology and Biotechnology, 64(2): 255-262.
Kester D R, Duedall I W, Connors D N et al. 1967. Preparation of artificial seawater. Limnology and Oceanography, 12(1): 176-179.
Kirstine W V, Galbally I E. 2012. Ethanol in the environment:a critical review of its roles as a natural product, a biofuel, and a potential environmental pollutant. Critical Reviews in Environmental Science and Technology, 42(16): 1735-1779.
Lin L A, Liu W W, Zhang M P et al. 2019. Different height forms of Spartina alterniflora might select their own Rhizospheric bacterial communities in southern coast of China. Microbial Ecology, 77(1): 124-135.
Matsudo M C, Sousa T F, Pérez-Mora L S et al. 2017. Ethanol as complementary carbon source in Scenedesmus obliquus cultivation. Journal of Chemical Technology & Biotechnology, 92(4): 781-786.
Mayali X. 2018. Editorial: metabolic interactions between bacteria and phytoplankton. Frontiers in Microbiology, 9: 727.
Menzyanova N G, Bozhkov A I, Sotnik N N. 2002. Influence of ethanol on the growth dynamics and metabolism of triacylglycerides and β-carotene in Dunaliella viridis Teod. International Journal on Algae, 4: 99-111.
Menzyanova N G, Bozhkov A I. 2003. Influence of ethanol on metabolism of algae. Growth dynamics, content of nucleic acids, proteins, and lipids in Chlorella vulgaris Beijer and Spirulina platensis (Nordst.) Geitl. Cells. International Journal on Algae, 5(3): 64-73.
Miazek K, Kratky L, Sulc R et al. 2017. Effect of organic solvents on microalgae growth, metabolism and industrial bioproduct extraction: a review. International Journal of Molecular Sciences, 18(7): 1429.
Milani M, Consoli S, Marzo A et al. 2020. Treatment of winery wastewater with a multistage constructed wetland system for irrigation reuse. Water, 12(5): 1260.
Mohammadkazemi F, Doosthoseini K, Azin M. 2015. Effect of ethanol and medium on bacterial cellulose (BC) production by Gluconacetobacter xylinus (PTCC 1734).Cellulose Chemistry and Technology, 49(5-6): 455-462.
Navakoudis E, Ioannidis N E, Dörnemann D et al. 2007.Changes in the LHCII-mediated energy utilization and dissipation adjust the methanol-induced biomass increase.Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1767(7): 948-955.
Ono K, Kawanaka Y, Izumi Y et al. 1995. Mitochondrial alcohol dehydrogenase from ethanol-grown Euglena gracilis. The Journal of Biochemistry, 117(6): 1178-1182.
Parks D H, Tyson G W, Hugenholtz P et al. 2014. STAMP:statistical analysis of taxonomic and functional profiles.Bioinformatics, 30(21): 3123-3124.
Pinhassi J, Sala M M, Havskum H et al. 2004. Changes in Bacterioplankton composition under different phytoplankton regimens. Applied and Environmental Microbiology, 70(11): 6753-6766.
Rideout J R, He Y, Navas-Molina J A et al. 2014.Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. PeerJ, 2: e545.
Rodriguez-Caballero A, Ramond J B, Welz P J et al. 2012.Treatment of high ethanol concentration wastewater by biological sand filters: enhanced COD removal and bacterial community dynamics. Journal of Environmental Management, 109: 54-60.
Rooney-Varga J N, Giewat M W, Savin M C et al. 2005.Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microbial Ecology, 49(1): 163-175.
Schäfer H, Abbas B, Witte H et al. 2002. Genetic diversity of ‘satellite’ bacteria present in cultures of marine diatoms.FEMS Microbiology Ecology, 42(1): 25-35.
Sharma B, Felix J D, Myles L T et al. 2021. Wet deposition ethanol concentration at US atmospheric integrated research monitoring network (AIRMoN) sites. Journal of Atmospheric Chemistry, 78(2): 125-138.
Shiraishi T, Fukusaki E I, Miyake C et al. 2000. Formate protects photosynthetic machinery from photoinhibition.Journal of Bioscience and Bioengineering, 89(6): 564-568.
Sison-Mangus M P, Jiang S, Kudela R M et al. 2016. Phytoplankton-associated bacterial community composition and succession during toxic diatom bloom and non-bloom events. Frontiers in Microbiology, 7: 1433.
Smith M G, Des Etages S G, Snyder M. 2004. Microbial synergy via an ethanol-triggered pathway. Molecular and Cellular Biology, 24(9): 3874-3884.
Stratton G W. 1987. Toxic effects of organic solvents on the growth of blue-green algae. Bulletin of Environmental Contamination and Toxicology, 38(6): 1012-1019.
Suggett D J, MacIntyre H L, Geider R J. 2004. Evaluation of biophysical and optical determinations of light absorption by photosystem II in phytoplankton. Limnology and Oceanography: Methods, 2(10): 316-332.
Takemura H, Kondo K, Horinouchi S et al. 1993. Induction by ethanol of alcohol dehydrogenase activity in Acetobacter pasteurianus. Journal of Bacteriology, 175(21): 6857-6866.
Tashiro Y, Inagaki A, Ono K et al. 2014. Low concentrations of ethanol stimulate biofilm and pellicle formation in Pseudomonas aeruginosa. Bioscience, Biotechnology, and Biochemistry, 78(1): 178-181.
Trcek J. 2005. Quick identification of acetic acid bacteria based on nucleotide sequences of the 16S-23S rDNA internal transcribed spacer region and of the PQQ-dependent alcohol dehydrogenase gene. Systematic and Applied Microbiology, 28(8): 735-745.
Varasteh T, Moreira A P B, Lima A W S et al. 2020. Genomic repertoire of Mameliella alba Ep20 associated with Symbiodinium from the endemic coral Mussismilia braziliensis. Symbiosis, 80(1): 53-60.
Willey J D, Avery G B, Felix J D et al. 2019. Rapidly increasing ethanol concentrations in rainwater and air. npj Climate and Atmospheric Science, 2(1): 3.
Wu C C, Wang W, Yue L et al. 2013. Enhancement effect of ethanol on lipid and fatty acid accumulation and composition of Scenedesmus sp. Bioresource Technology, 140: 120-125.
Yao S, Lyu S, An Y et al. 2019. Microalgae‐bacteria symbiosis in microalgal growth and biofuel production: a review.Journal of Applied Microbiology, 126(2): 359-368.
Zobell C E, Cobet A B. 1964. Filament formation by Escherichia coli at increased hydrostatic pressures.Journal of Bacteriology, 87(3): 710-719.
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