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Untargeted metabolomic analysis reveals the mechanism of Enterococcus faecium agent induced CaCO3 scale inhibition

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Abstract

In this study, a lactic acid bacterium, Enterococcus faecium, was found to prevent CaCO3 precipitation through its metabolism. On analysis of all stages of E. faecium growth, static jar tests demonstrated that stationary phase E. faecium broth possessed the highest inhibition efficiency of 97.3% at a 0.4% inoculation dosage, followed by the decline and log phases with efficiencies of 90.03% and 76.07%, respectively. Biomineralization experiments indicated that E. faecium fermented the substrate to produce organic acid, which resulted in modulation of the pH and alkalinity of the environment and thus inhibited CaCO3 precipitation. Surface characterization techniques indicated that the CaCO3 crystals precipitated by the E. faecium broth tended to be significantly distorted and formed other organogenic calcite crystals. The scale inhibition mechanisms were revealed by untargeted metabolomic analysis on log and stationary phase E. faecium broth. In total, 264 metabolites were detected, 28 of which were differential metabolites (VIP ≥ 1 and p < 0.05). Of these, 15 metabolites were upregulated in stationary phase broth, and 13 metabolites were downregulated in log phase broth. Metabolic pathway analysis suggested that improved glycolysis and the TCA cycle were the main reasons for enhancement of the antiscaling performance of E. faecium broth. These findings have significant implications for microbial metabolism-induced CaCO3 scale inhibition.

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Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Beauprez JJ, De Mey M, Soetaert WK (2010) Microbial succinic acid production: natural versus metabolic engineered producers. Process Biochem 45:1103–1114

    Article  CAS  Google Scholar 

  • Beresford TP (2022) Lactic acid bacteria: citrate fermentation. In: McSweeney PLH, McNamara JP, McSweeney PLH, McNamara JP, McSweeney PLH, McNamara JPS (eds) Encyclopedia of Dairy Sciences, 3rd edn. Academic Press, Oxford, pp 144–150

    Chapter  Google Scholar 

  • Bo F, Palmgren R, Keiding K, Nielsen PH (1996) Extraction of extracellular polymers from activated sludge using a cation exchange resin. Water Res 30:1749–1758

    Article  Google Scholar 

  • Bundeleva IA, Shirokova LS, Pokrovsky OS, Bénézeth P, Ménez B, Gérard E, Balor S (2014) Experimental modeling of calcium carbonate precipitation by cyanobacterium Gloeocapsa sp. Chem Geol 374–375:44–60

    Article  Google Scholar 

  • Cai L, Wang W, Tong J, Fang L, He X, Xue Q, Li Y (2022) Changes of bioactive substances in lactic acid bacteria and yeasts fermented kiwifruit extract during the fermentation. LWT 164:113629

    Article  CAS  Google Scholar 

  • Chauhan K, Kumar R, Kumar M, Sharma P, Chauhan GS (2012) Modified pectin-based polymers as green antiscalants for calcium sulfate scale inhibition. Desalination 305:31–37

    Article  CAS  Google Scholar 

  • Chaussemier M, Pourmohtasham E, Gelus D, Pécoul N, Perrot H, Lédion J, Cheap-Charpentier H, Horner O (2015) State of art of natural inhibitors of calcium carbonate scaling a review article. Desalination 356:47–55

    Article  CAS  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

    Article  CAS  Google Scholar 

  • Chrysi S, Laspidou BER (2002) A unified theory for extracellular polymeric substances, soluble microbial products, and active and inert biomass. Water Res 36:2711–2720

    Article  Google Scholar 

  • Deb A, Gurung K, Rumky J, Sillanpää M, Mänttäri M, Kallioinen M (2022) Dynamics of microbial community and their effects on membrane fouling in an anoxic-oxic gravity-driven membrane bioreactor under varying solid retention time: a pilot-scale study. Sci Total Environ 807:150878

    Article  CAS  Google Scholar 

  • Foulquié Moreno MR, Sarantinopoulos P, Tsakalidou E, De Vuyst L (2006) The role and application of enterococci in food and health. Int J Food Microbiol 106:1–24

    Article  Google Scholar 

  • Gänzle MG, Vermeulen N, Vogel RF (2007) Carbohydrate, peptide and lipid metabolism of lactic acid bacteria in sourdough. Food Microbiol 24:128–138

    Article  Google Scholar 

  • Gao Y, Fan L, Ward L, Liu Z (2015) Synthesis of polyaspartic acid derivative and evaluation of its corrosion and scale inhibition performance in seawater utilization. Desalination 365:220–226

    Article  CAS  Google Scholar 

  • Gao R, Li Y, Zhu T, Dai Y, Li X, Wang L, Li L, Qu Q (2021) ZIF-8@s-EPS as a novel hydrophilic multifunctional biomaterial for efficient scale inhibition, antibacterial and antifouling in water treatment. Sci Total Environ 773:145706

    Article  CAS  Google Scholar 

  • Han Y, Lo Y, Cheng C, Yu W, Nagarajan D, Liu C, Li Y, Chang J (2017) Calcium ion adsorption with extracellular proteins of thermophilic bacteria isolated from geothermal sites—a feasibility study. Biochem Eng J 117:48–56

    Article  CAS  Google Scholar 

  • Hanniffy SB, Peláez C, Martínez-Bartolomé MA, Requena T, Martínez-Cuesta MC (2009) Key enzymes involved in methionine catabolism by cheese lactic acid bacteria. Int J Food Microbiol 135:223–230

    Article  CAS  Google Scholar 

  • Hasson D, Shemer H, Sher A (2011) State of the art of friendly “green” scale control inhibitors: a review article. Ind Eng Chem Res 50:7601–7607

    Article  CAS  Google Scholar 

  • Hoch AR, Reddy MM, Aiken GR (2000) Calcite crystal growth inhibition by humic substances with emphasis on hydrophobic acids from the Florida Everglades. Geochim Cosmochim Acta 64:61–72

    Article  CAS  Google Scholar 

  • Hu Y, Chen C, Liu S (2022) Evaluation of microbial agents as corrosion and scale inhibitor for industrial cooling water applications. Water Sci Technol 85:1904–1919

    Article  CAS  Google Scholar 

  • Juillard V, Lopez-Kleine L, Monnet V (2022) Lactic acid bacteria: proteolytic systems. In: McSweeney PLH, McNamara JP, McSweeney PLH, McNamara JP, McSweeney PLH, McNamara JPS (eds) Encyclopedia of Dairy Sciences, 3rd edn. Academic Press, Oxford, pp 249–255

    Chapter  Google Scholar 

  • Kawaguchi T, Decho AW (2002) Isolation and biochemical characterization of extracellular polymeric secretions (EPS) from modern soft marine stromatolites (Bahamas) and its inhibitory effect on CaCO3 precipitation. Prep Biochem Biotech 32:51–63

    Article  CAS  Google Scholar 

  • Kühn I, Iversen A, Burman LG, Olsson-Liljequist B, Franklin A, Finn M, Aarestrup F, Seyfarth AM, Blanch AR, Vilanova X, Taylor H, Caplin J, Moreno MA, Dominguez L, Herrero IA, Möllby R (2003) Comparison of enterococcal populations in animals, humans, and the environment - a European study. Int J Food Microbiol 88:133–145

    Article  Google Scholar 

  • Kulikova NA, Perminova IV (2021) Interactions between humic substances and microorganisms and their implications for nature-like bioremediation technologies. Molecules 26:2706

    Article  CAS  Google Scholar 

  • Kumar T, Vishwanatham S, Kundu SS (2010) A laboratory study on pteroyl-l-glutamic acid as a scale prevention inhibitor of calcium carbonate in aqueous solution of synthetic produced water. J Petrol Sci Eng 71:1–7

    Article  CAS  Google Scholar 

  • Li W, Yu L, Wu Y, Jia L, Yuan D (2007) Enhancement of Ca2+ release from limestone by microbial extracellular carbonic anhydrase. Bioresource Technol 98:950–953

    Article  CAS  Google Scholar 

  • Li S, Qu Q, Li L, Xia K, Li Y, Zhu T (2019) Bacillus cereus s-EPS as a dual bio-functional corrosion and scale inhibitor in artificial seawater. Water Res 166:115094

    Article  CAS  Google Scholar 

  • Lian B, Chen Y, Zhu L, Yang R (2008) Effect of microbial weathering on carbonate rocks. Earth Sci Front 15:90–99

    Article  Google Scholar 

  • Liang A, Paulo C, Zhu Y, Dittrich M (2013) CaCO3 biomineralization on cyanobacterial surfaces: insights from experiments with three Synechococcus strains. Colloids Surf, B 111:600–608

    Article  CAS  Google Scholar 

  • Liu Y, Zou C, Li C, Lin L, Chen W (2016) Evaluation of β-cyclodextrin–polyethylene glycol as green scale inhibitors for produced-water in shale gas well. Desalination 377:28–33

    Article  CAS  Google Scholar 

  • Loften JR, Linn JG, Drackley JK, Jenkins TC, Soderholm CG, Kertz AF (2014) Invited review: palmitic and stearic acid metabolism in lactating dairy cows. J Dairy Sci 97:4661–4674

    Article  CAS  Google Scholar 

  • Macedo RGMD, Marques NDN, Paulucci LCS, Cunha JVM, Villetti MA, Castro BB, Balaban RDC (2019) Water-soluble carboxymethylchitosan as green scale inhibitor in oil wells. Carbohyd Polym 215:137–142

    Article  CAS  Google Scholar 

  • Martinez RE, Weber S, Grimm C (2016) Effects of freshwater Synechococcus sp. cyanobacteria pH buffering on CaCO3 precipitation: implications for CO2 sequestration. Appl Geochem 75:76–89

    Article  CAS  Google Scholar 

  • Mucchetti G, Locci F, Massara P, Vitale R, Neviani E (2002) Production of pyroglutamic acid by thermophilic lactic acid bacteria in hard-cooked mini-cheeses. J Dairy Sci 85:2489–2496

    Article  CAS  Google Scholar 

  • Nascimento MF, Marques N, Correia J, Faria NT, Mira NP, Ferreira FC (2022) Integrated perspective on microbe-based production of itaconic acid: from metabolic and strain engineering to upstream and downstream strategies. Process Biochem 117:53–67

    Article  CAS  Google Scholar 

  • Nzle G, Michael G (2015) Lactic metabolism revisited: metabolism of lactic acid bacteria in food fermentations and food spoilage. Curr Opin Food Sci 2:106–117

    Article  Google Scholar 

  • Özcelik S, Kuley E, Özogul F (2016) Formation of lactic, acetic, succinic, propionic, formic and butyric acid by lactic acid bacteria. LWT 73:536–542

    Article  Google Scholar 

  • Perez RH, Zendo T, Sonomoto K (2022) Multiple bacteriocin production in lactic acid bacteria. J Biosci Bioeng 134:277–287

    Article  CAS  Google Scholar 

  • Punia Bangar S, Suri S, Trif M, Ozogul F (2022) Organic acids production from lactic acid bacteria: a preservation approach. Food Biosci 46:101615

    Article  CAS  Google Scholar 

  • Rea MC, Cogan TM (2003) Glucose prevents citrate metabolism by enterococci. Int J Food Microbiol 88:201–206

    Article  CAS  Google Scholar 

  • Rosenberg J, Ischebeck T, Commichau FM (2017) Vitamin B6 metabolism in microbes and approaches for fermentative production. Biotechnol Adv 35:31–40

    Article  CAS  Google Scholar 

  • Sajjad M, Kim KS (2015) Studies on the interactions of Ca2+ and Mg2+ with EPS and their role in determining the physicochemical characteristics of granular sludges in SBR system. Process Biochem 50:966–972

    Article  CAS  Google Scholar 

  • Santos VHJM, Pontin D, Ponzi GGD, Stepanha ASDG, Martel RB, Schütz MK, Einloft SMO, Dalla Vecchia F (2021) Application of Fourier transform infrared spectroscopy (FTIR) coupled with multivariate regression for calcium carbonate (CaCO3) quantification in cement. Constr Build Mater 313:125413

    Article  Google Scholar 

  • Sarantinopoulos P, Makras L, Vaningelgem F, Kalantzopoulos G, De Vuyst L, Tsakalidou E (2003) Growth and energy generation by Enterococcus faecium FAIR-E 198 during citrate metabolism. Int J Food Microbiol 84:197–206

    Article  CAS  Google Scholar 

  • Shakkthivel P, Vasudevan T (2006) Acrylic acid-diphenylamine sulphonic acid copolymer threshold inhibitor for sulphate and carbonate scales in cooling water systems. Desalination 197:179–189

    Article  CAS  Google Scholar 

  • Sharma A, Gupta G, Ahmad T, Kaur B, Hakeem KR (2020) Tailoring cellular metabolism in lactic acid bacteria through metabolic engineering. J Microbiol Meth 170:105862

    Article  CAS  Google Scholar 

  • Shi W, Ding C, Yan J, Han X, Lv Z, Lei W, Xia M, Wang F (2012) Molecular dynamics simulation for interaction of PESA and acrylic copolymers with calcite crystal surfaces. Desalination 291:8–14

    Article  CAS  Google Scholar 

  • Touir R, Dkhireche N, Ebn Touhami M, Lakhrissi M, Lakhrissi B, Sfaira M (2009) Corrosion and scale processes and their inhibition in simulated cooling water systems by monosaccharides derivatives. Desalination 249:922–928

    Article  CAS  Google Scholar 

  • Tymoszewska A, Diep DB, Aleksandrzak-Piekarczyk T (2018) The extracellular loop of Man-PTS subunit IID is responsible for the sensitivity of Lactococcus garvieae to garvicins A, B and C. Sci Rep-UK 8(1). https://doi.org/10.1038/s41598-018-34087-2

  • Valledor SJD, Dioso CM, Bucheli JEV, Park YJ, Suh DH, Jung ES, Kim B, Holzapfel WH, Todorov SD (2022) Characterization and safety evaluation of two beneficial, enterocin-producing Enterococcus faecium strains isolated from kimchi, a Korean fermented cabbage. Food Microbiol 102:103886

    Article  CAS  Google Scholar 

  • Wang M, Liu Y, Wang S, Wang K, Zhang Y (2021) Development of a compound microbial agent beneficial to the composting of Chinese medicinal herbal residues. Bioresource Technol 330:124948

    Article  CAS  Google Scholar 

  • Wei Y, Han CS, Zhou J, Liu Y, Chen L, He RQ (2012) d-ribose in glycation and protein aggregation. Biochimica et Biophysica Acta (BBA)-Gen Subjects 1820:488–494

    Article  CAS  Google Scholar 

  • Wei T, Fang Q, Luo J, Chen Y, Zhang K (2021) Insight into effects of long-chain fatty acids on propionic acid production in anaerobic fermentation: a case study of oleic acid and palmitic acid. J Water Process Eng 44:102415

    Article  Google Scholar 

  • Wilén B, Jin B, Lant P (2003) The influence of key chemical constituents in activated sludge on surface and flocculating properties. Water Res 37:2127–2139

    Article  Google Scholar 

  • Yu W, Wang Y, Li A, Yang H (2018) Evaluation of the structural morphology of starch-graft-poly(acrylic acid) on its scale-inhibition efficiency. Water Res 141:86–95

    Article  CAS  Google Scholar 

  • Zhang Y, Yin H, Zhang Q, Li Y, Yao P (2016) Synthesis and characterization of novel polyaspartic acid/urea graft copolymer with acylamino group and its scale inhibition performance. Desalination 395:92–98

    Article  CAS  Google Scholar 

  • Zhao Y, Xu Z, Wang B, He J (2019) Scale inhibition performance of sodium carboxymethyl cellulose on heat transfer surface at various temperatures: experiments and molecular dynamics simulation. Int J Heat Mass Tran 141:457–463

    Article  CAS  Google Scholar 

  • Zhao M, Bai X, Zhang Y, Yuan Y, Sun J (2022) Enhanced photodegradation of antibiotics based on anoxygenic photosynthetic bacteria and bacterial metabolites: a sustainably green strategy for the removal of high-risk organics from secondary effluent. J Hazard Mater 430:128350

    Article  CAS  Google Scholar 

  • Zheng T, Qian C (2020) Influencing factors and formation mechanism of CaCO3 precipitation induced by microbial carbonic anhydrase. Process Biochem 91:271–281

    Article  CAS  Google Scholar 

  • Zhuang D, Yan H, Tucker ME, Zhao H, Han Z, Zhao Y, Sun B, Li D, Pan J, Zhao Y, Meng R, Shan G, Zhang X, Tang R (2018) Calcite precipitation induced by Bacillus cereus MRR2 cultured at different Ca2+ concentrations: further insights into biotic and abiotic calcite. Chem Geol 500:64–87

    Article  CAS  Google Scholar 

  • Zou S, Zhang Z, Zhao K, Liu Z, Zheng Y (2022) Metabolic engineering of Escherichia coli for improved d-pantothenic acid biosynthesis by enhancing NADPH availability. Biochem Eng J 187:108603

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Hebei Key Lab of Power Plant Flue Gas Multi-Pollutants Control, Department of Environmental Science and Engineering, North China Electric Power University, Baoding, 071003, People’s Republic of China

    Yanglin Hu, Chuanmin Chen, Songtao Liu, Wenbo Jia & Yue Cao

  2. MOE Key Laboratory of Resources and Environmental Systems Optimization, College of Environmental Science and Engineering, North China Electric Power University, Beijing, 102206, People’s Republic of China

    Yanglin Hu, Chuanmin Chen, Songtao Liu, Wenbo Jia & Yue Cao

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  1. Yanglin Hu
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  2. Chuanmin Chen
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  3. Songtao Liu
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Contributions

Yanglin Hu: Conceptualization, methodology, investigation, formal analysis, visualization, writing—original draft, writing—revision. Chuanmin Chen: Conceptualization, methodology, investigation, validation, supervision, formal analysis, resources, project administration. Songtao Liu: Resources, validation, supervision. Wenbo Jia: Resources, validation, supervision. Yue Cao: Resources, validation, supervision.

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Correspondence to Chuanmin Chen.

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Hu, Y., Chen, C., Liu, S. et al. Untargeted metabolomic analysis reveals the mechanism of Enterococcus faecium agent induced CaCO3 scale inhibition. Environ Sci Pollut Res 30, 69205–69220 (2023). https://doi.org/10.1007/s11356-023-27314-5

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