Developing a Fluorescent Inducible System for Free Fucose Quantification in Escherichia coli
Abstract
:1. Introduction
2. Materials and Methods
3. Results
3.1. Biosensor Properties and Functions
3.2. Comparison of Biosensor Specificities
3.3. Calibration Curves
3.4. Sensitivity of the E. coli BL21 pFuc+FucR colE1 Biosensor
3.5. Measuring Fucose in the Supernatant of B. bifidum JCM1254
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Schneider, M.; Al-Shareffi, E.; Haltiwanger, R.S. Biological functions of fucose in mammals. Glycobiology 2017, 27, 601–618. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Becker, D.J.; Lowe, J.B. Fucose: Biosynthesis and biological function in mammals. Glycobiology 2003, 13, 41R–53R. [Google Scholar] [CrossRef]
- González-Morelo, K.J.; Vega-Sagardía, M.; Garrido, D. Molecular Insights Into O-Linked Glycan Utilization by Gut Microbes. Front. Microbiol. 2020, 11, 591568. [Google Scholar] [CrossRef]
- Varki, A.; Lowe, J.B. Biological roles of glycans. In Essentials of Glycobiology; Varki, A., Cummings, R., Esko, J., Eds.; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA, 2009. [Google Scholar]
- Goto, Y.; Uematsu, S.; Kiyono, H. Epithelial glycosylation in gut homeostasis and inflammation. Nat. Immunol. 2016, 17, 1244–1251. [Google Scholar] [CrossRef] [PubMed]
- Sela, D.A.; Garrido, D.; Lerno, L.; Wu, S.; Tan, K.; Eom, H.-J.; Joachimiak, A.; Lebrilla, C.B.; Mills, D.A. Bifidobacterium longum subsp. infantis ATCC 15697 α-fucosidases are active on fucosylated human milk oligosaccharides. Appl. Environ. Microbiol. 2012, 78, 795–803. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ojima, M.N.; Asao, Y.; Nakajima, A.; Katoh, T.; Kitaoka, M.; Gotoh, A.; Hirose, J.; Urashima, T.; Fukiya, S.; Yokota, A.; et al. Diversification of a Fucosyllactose Transporter within the Genus Bifidobacterium. Appl. Environ. Microbiol. 2022, 88, e01437-21. [Google Scholar] [CrossRef]
- Marcobal, A.; Barboza, M.; Sonnenburg, E.D.; Pudlo, N.; Martens, E.C.; Desai, P.; Lebrilla, C.B.; Weimer, B.C.; Mills, D.A.; German, J.B.; et al. Bacteroides in the Infant Gut Consume Milk Oligosaccharides via Mucus-Utilization Pathways. Cell Host Microbe 2011, 10, 507–514. [Google Scholar] [CrossRef] [Green Version]
- Ruiz-Moyano, S.; Totten, S.M.; Garrido, D.A.; Smilowitz, J.T.; Bruce German, J.; Lebrilla, C.B.; Mills, D.A. Variation in consumption of human milk oligosaccharides by infant gut-associated strains of bifidobacterium breve. Appl. Environ. Microbiol. 2013, 79, 6040–6049. [Google Scholar] [CrossRef] [Green Version]
- Hooper, L.V.; Xu, J.; Falk, P.G.; Midtvedt, T.; Gordon, J.I. A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc. Natl. Acad. Sci. USA 1999, 96, 9833–9838. [Google Scholar] [CrossRef] [Green Version]
- Gotoh, A.; Katoh, T.; Sakanaka, M.; Ling, Y.; Yamada, C.; Asakuma, S.; Urashima, T.; Tomabechi, Y.; Katayama-Ikegami, A.; Kurihara, S.; et al. Sharing of human milk oligosaccharides degradants within bifidobacterial communities in faecal cultures supplemented with Bifidobacterium bifidum. Sci. Rep. 2018, 8, 13958. [Google Scholar] [CrossRef] [Green Version]
- Tsukuda, N.; Yahagi, K.; Hara, T.; Watanabe, Y.; Matsumoto, H.; Mori, H.; Higashi, K.; Tsuji, H.; Matsumoto, S.; Kurokawa, K.; et al. Key bacterial taxa and metabolic pathways affecting gut short-chain fatty acid profiles in early life. ISME J. 2021, 15, 2574–2590. [Google Scholar] [CrossRef] [PubMed]
- Bunesova, V.; Lacroix, C.; Schwab, C. Mucin Cross-Feeding of Infant Bifidobacteria and Eubacterium hallii. Microb. Ecol. 2018, 75, 228–238. [Google Scholar] [CrossRef] [PubMed]
- Pacheco, A.R.; Munera, D.; Waldor, M.K.; Sperandio, V.; Ritchie, J.M. Fucose sensing regulates bacterial intestinal colonization. Nature 2012, 492, 113–117. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pickard, J.M.; Chervonsky, A.V. Intestinal Fucose as a Mediator of Host–Microbe Symbiosis. J. Immunol. 2015, 194, 5588–5593. [Google Scholar] [CrossRef] [Green Version]
- Pickard, J.M.; Maurice, C.F.; Kinnebrew, M.A.; Abt, M.C.; Schenten, D.; Golovkina, T.V.; Bogatyrev, S.R.; Ismagilov, R.F.; Pamer, E.G.; Turnbaugh, P.J.; et al. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 2014, 514, 638–641. [Google Scholar] [CrossRef] [Green Version]
- Furniss, R.C.D.; Clements, A. Regulation of the locus of enterocyte effacement in attaching and effacing pathogens. J. Bacteriol. 2018, 200, e00336-17. [Google Scholar] [CrossRef] [Green Version]
- Gibson, G.R.; McCartney, A.L.; Rastall, R.A. Prebiotics and resistance to gastrointestinal infections. Br. J. Nutr. 2005, 93, S31–S34. [Google Scholar] [CrossRef]
- Yamauchi, M.; Nishikawa, F.; Kimura, K.; Maezawa, Y.; Ohata, M.; Toda, G. Urinaryl-fucose: A new marker for the diagnosis of chronic liver disease. Int. Hepatol. Commun. 1993, 1, 222–227. [Google Scholar] [CrossRef]
- Tsiafoulis, C.G.; Prodromidis, M.I.; Karayannis, M.I. Development of an amperometric biosensing method for the determination of L-fucose in pretreated urine. Biosens. Bioelectron. 2004, 20, 620–627. [Google Scholar] [CrossRef]
- McGovern, D.P.B.; Jones, M.R.; Taylor, K.D.; Marciante, K.; Yan, X.; Dubinsky, M.; Ippoliti, A.; Vasiliauskas, E.; Berel, D.; Derkowski, C.; et al. Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn’s disease. Hum. Mol. Genet. 2010, 19, 3468–3476. [Google Scholar] [CrossRef] [Green Version]
- Wang, H.; Walaszczyk, E.J.; Li, K.; Chung-Davidson, Y.-W.; Li, W. High-performance liquid chromatography with fluorescence detection and ultra-performance liquid chromatography with electrospray tandem mass spectrometry method for the determination of indoleamine neurotransmitters and their metabolites in sea lamprey plasma. Anal. Chim. Acta 2012, 721, 147–153. [Google Scholar] [CrossRef]
- Chen, Y.; Yao, Q.; Zeng, X.; Hao, C.; Li, X.; Zhang, L.; Zeng, P. Determination of monosaccharide composition in human serum by an improved HPLC method and its application as candidate biomarkers for endometrial cancer. Front. Oncol. 2022, 12, 1014159. [Google Scholar] [CrossRef] [PubMed]
- Suzuki, J.; Kondo, A.; Kato, I.; Hase, S.; Ikenaka, T. Assay of urinary free fucose by fluorescence labeling and high-performance liquid chromatography. Clin. Chem. 1992, 38, 752–755. [Google Scholar] [CrossRef] [PubMed]
- Chaturvedi, P.; Warren, C.D.; Altaye, M.; Morrow, A.L.; Ruiz-Palacios, G.; Pickering, L.K.; Newburg, D.S. Fucosylated human milk oligosaccharides vary between individuals and over the course of lactation. Glycobiology 2001, 11, 365–372. [Google Scholar] [CrossRef] [PubMed]
- Sakai, T.; Yamamoto, K.; Yokota, H.; Hakozaki-Usui, K.; Hino, F.; Kato, I. Rapid, simple enzymatic assay of free L-fucose in serum and urine, and its use as a marker for cancer, cirrhosis, and gastric ulcers. Clin. Chem. 1990, 36, 474–476. [Google Scholar] [CrossRef]
- Erlandsson, P.G.; Åström, E.; Påhlsson, P.; Robinson, N.D. Determination of Fucose Concentration in a Lectin-Based Displacement Microfluidic Assay. Appl. Biochem. Biotechnol. 2019, 188, 868–877. [Google Scholar] [CrossRef] [Green Version]
- Gao, Z.; Chen, S.; Du, J.; Wu, Z.; Ge, W.; Gao, S.; Zhou, Z.; Yang, X.; Xing, Y.; Shi, M.; et al. Quantitative analysis of fucosylated glycoproteins by immobilized lectin-affinity fluorescent labeling. RSC Adv. 2023, 13, 6676–6687. [Google Scholar] [CrossRef]
- Thurl, S.; Müller-Werner, B.; Sawatzki, G. Quantifbation of individual oligosaccharide compounds from human milk using high-pH anion-exchange chromatography. Anal. Biochem. 1996, 235, 202–206. [Google Scholar] [CrossRef]
- Shin, J.; Park, M.; Kim, C.; Kim, H.; Park, Y.; Ban, C.; Yoon, J.W.; Shin, C.S.; Lee, J.W.; Jin, Y.S.; et al. Development of fluorescent Escherichia coli for a whole-cell sensor of 2′-fucosyllactose. Sci. Rep. 2020, 10, 10514. [Google Scholar] [CrossRef]
- Della Corte, D.; van Beek, H.L.; Syberg, F.; Schallmey, M.; Tobola, F.; Cormann, K.U.; Schlicker, C.; Baumann, P.T.; Krumbach, K.; Sokolowsky, S.; et al. Engineering and application of a biosensor with focused ligand specificity. Nat. Commun. 2020, 11, 4851. [Google Scholar] [CrossRef]
- Barra, M.; Danino, T.; Garrido, D. Engineered Probiotics for Detection and Treatment of Inflammatory Intestinal Diseases. Front. Bioeng. Biotechnol. 2020, 8, 265. [Google Scholar] [CrossRef] [Green Version]
- Sharma, S.; Kumar, R.; Jain, A.; Kumar, M.; Gauttam, R.; Banerjee, R.; Mukhopadhyay, J.; Tyagi, J.S. Functional insights into Mycobacterium tuberculosis DevR-dependent transcriptional machinery utilizing Escherichia coli. Biochem. J. 2021, 478, 3079–3098. [Google Scholar] [CrossRef] [PubMed]
- Pierre, M.; Julien, P.; Fabien, L. Functional Analysis of Deoxyhexose Sugar Utilization in Escherichia coli Reveals Fermentative Metabolism under Aerobic Conditions. Appl. Environ. Microbiol. 2021, 87, e00719-21. [Google Scholar] [CrossRef]
- Kim, J.; Cheong, Y.E.; Jung, I.; Kim, K.H. Metabolomic and transcriptomic analyses of Escherichia coli for efficient fermentation of L-Fucose. Mar. Drugs 2019, 17, 82. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bartkus, J.M.; Mortlock, R.P. Isolation of a mutation resulting in constitutive synthesis of L-fucose catabolic enzymes. J. Bacteriol. 1986, 165, 710–714. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, Y.-M.; Zhu, Y.; Lin, E.C.C. The organization of the fuc regulon specifying l-fucose dissimilation in Escherichia coli K12 as determined by gene cloning. Mol. Gen. Genet. MGG 1987, 210, 331–337. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Y.; Lin, E.C. A mutant crp allele that differentially activates the operons of the fuc regulon in Escherichia coli. J. Bacteriol. 1988, 170, 2352–2358. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Medina, D.A.; Pinto, F.; Ovalle, A.; Thomson, P.; Garrido, D. Prebiotics mediate microbial interactions in a consortium of the infant gut microbiome. Int. J. Mol. Sci. 2017, 18, 2095. [Google Scholar] [CrossRef] [Green Version]
- Pédelacq, J.-D.; Cabantous, S.; Tran, T.; Terwilliger, T.C.; Waldo, G.S. Engineering and characterization of a superfolder green fluorescent protein. Nat. Biotechnol. 2006, 24, 79–88. [Google Scholar] [CrossRef]
- Madar, D.; Dekel, E.; Bren, A.; Alon, U. Negative auto-regulation increases the input dynamic-range of the arabinose system of Escherichia coli. BMC Syst. Biol. 2011, 5, e111. [Google Scholar] [CrossRef] [Green Version]
- Alon, U. An Introduction to Systems Biology: Design Principles of Biological Circuits, 1st ed.; Chapman and Hall: London, UK; CRC: Boca Raton, FL, USA, 2006. [Google Scholar]
- Mangan, S.; Itzkovitz, S.; Zaslaver, A.; Alon, U. The Incoherent Feed-forward Loop Accelerates the Response-time of the gal System of Escherichia coli. J. Mol. Biol. 2006, 356, 1073–1081. [Google Scholar] [CrossRef] [PubMed]
- Aidelberg, G.; Towbin, B.D.; Rothschild, D.; Dekel, E.; Bren, A.; Alon, U. Hierarchy of non-glucose sugars in Escherichia coli. BMC Syst. Biol. 2014, 8, e133. [Google Scholar] [CrossRef] [Green Version]
- Beisel, C.L.; Storz, G. The Base-Pairing RNA Spot 42 Participates in a Multioutput Feedforward Loop to Help Enact Catabolite Repression in Escherichia coli. Mol. Cell 2011, 41, 286–297. [Google Scholar] [CrossRef] [Green Version]
- Chen, Y.M.; Tobin, J.F.; Zhu, Y.; Schleif, R.F.; Lin, E.C. Cross-induction of the L-fucose system by L-rhamnose in Escherichia coli. J. Bacteriol. 1987, 169, 3712–3719. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gottesman, S. Proteases and their targets in Escherichia coli. Annu. Rev. Genet. 1996, 30, 465–506. [Google Scholar] [CrossRef] [PubMed]
- Coffey, J.W.; Miller, O.N.; Sellinger, O.Z. The Metabolism of l-Fucose in the Rat. J. Biol. Chem. 1964, 239, 4011–4017. [Google Scholar] [CrossRef]
- Stepien, K.M.; Ciara, E.; Jezela-Stanek, A. Fucosidosis—Clinical Manifestation, Long-Term Outcomes, and Genetic Profile—Review and Case Series. Genes 2020, 11, 1383. [Google Scholar] [CrossRef]
- Wang, H.; Zhang, X.; Peng, Y.; Pan, B.; Wang, B.; Peng, D.H.; Guo, W. A LC-MS/MS method to simultaneously profile 14 free monosaccharides in biofluids. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2022, 1192, 123086. [Google Scholar] [CrossRef]
- Li, M.; Luo, Y.; Hu, M.; Li, C.; Liu, Z.; Zhang, T. Module-Guided Metabolic Rewiring for Fucosyllactose Biosynthesis in Engineered Escherichia coli with Lactose De Novo Pathway. J. Agric. Food Chem. 2022, 70, 14761–14770. [Google Scholar] [CrossRef]
- Crost, E.H.; Tailford, L.E.; Le Gall, G.; Fons, M.; Henrissat, B.; Juge, N. Utilisation of Mucin Glycans by the Human Gut Symbiont Ruminococcus gnavus Is Strain-Dependent. PLoS ONE 2013, 8, e76341. [Google Scholar] [CrossRef] [Green Version]
- Everard, A.; Belzer, C.; Geurts, L.; Ouwerkerk, J.P.; Druart, C.; Bindels, L.B.; Guiot, Y.; Derrien, M.; Muccioli, G.G.; Delzenne, N.M.; et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA 2013, 110, 9066–9071. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Plasmids | Antibiotic | Description | |
---|---|---|---|
1 | Pfuc sfGFP_ColE1 | Ampicillin | High-copy plasmid colE1 with fucose promoter and sfGFP with an ampicillin resistance gene. |
2 | Pfuc sfGFP_SC101 | Chloramphenicol | Low-copy plasmid SC101 with fucose promoter and sfGFP with a chloramphenicol resistance gene. |
3 | Pfuc+FucR1_colE1 | Ampicillin | High-copy plasmid colE1 with transcription factor FucR, fucose promoter and sfGFP with an ampicillin resistance gene |
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Nuñez, S.; Barra, M.; Garrido, D. Developing a Fluorescent Inducible System for Free Fucose Quantification in Escherichia coli. Biosensors 2023, 13, 388. https://doi.org/10.3390/bios13030388
Nuñez S, Barra M, Garrido D. Developing a Fluorescent Inducible System for Free Fucose Quantification in Escherichia coli. Biosensors. 2023; 13(3):388. https://doi.org/10.3390/bios13030388
Chicago/Turabian StyleNuñez, Samantha, Maria Barra, and Daniel Garrido. 2023. "Developing a Fluorescent Inducible System for Free Fucose Quantification in Escherichia coli" Biosensors 13, no. 3: 388. https://doi.org/10.3390/bios13030388