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Characterization and synthetic biology elements of nonmodel bacteria, Acetobacteraceae

  • Province Hefei National Laboratory for Physical Sciences at the Microscale, University of Science and Technology of China, Hefei 230026, China

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CSTR: 32290.14.JUSTC-2024-0044
https://doi.org/10.52396/JUSTC-2024-0044
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  • Author Bio:

    Yanmei Gao is a postdoctoral fellow at the University of Science and Technology of China. She received her Ph.D. degree from the University of Science and Technology of China in 2023. Her research mainly focuses on bacterial gene circuits to design and program engineered bacteria for the treatment of wound infections

  • Corresponding author: E-mail: ymg@mail.ustc.edu.cn
  • Received Date: 21 March 2024
  • Accepted Date: 08 May 2024
    Abstract

  • Abstract

    Acetobacteraceae has garnered significant attention because of its unique properties and the broad applications of the bacterial cellulose it produces. However, unlike model strains, Acetobacteraceae have few synthetic biology applications because they are difficult to manipulate genetically and have insufficient genetic regulatory elements, among other factors. To address this limitation, this study characterized the fundamental properties and synthetic biology elements of three commonly used bacterial cellulose-producing strains. First, the basic characteristics of the three strains, including their cellulose film production ability, division time, antibiotic susceptibility, and plasmid features, were analyzed. Two inducible promoters (pTrc and pLux101) were subsequently characterized within the three strains. The inducibility of the pTrc promoter was relatively low across the three strains (induction ratio: 1.98–6.39), whereas the pLux101 promoter demonstrated a significantly greater level of inducibility within the three strains (induction ratio: 87.28–216.71). Finally, through gene knockout experiments, this study identified four genes essential for bacterial cellulose film production in the genome of the Gluconacetobacter hansenii ATCC 5358 strain. This study not only enriches the library of synthetic biology elements in nonmodel strains, but also lays the foundation for the synthetic biology applications of Acetobacteraceae.

    Graphical abstract

    Characterization and synthetic biology element of Acetobacteraceae.

    Abstract

    Acetobacteraceae has garnered significant attention because of its unique properties and the broad applications of the bacterial cellulose it produces. However, unlike model strains, Acetobacteraceae have few synthetic biology applications because they are difficult to manipulate genetically and have insufficient genetic regulatory elements, among other factors. To address this limitation, this study characterized the fundamental properties and synthetic biology elements of three commonly used bacterial cellulose-producing strains. First, the basic characteristics of the three strains, including their cellulose film production ability, division time, antibiotic susceptibility, and plasmid features, were analyzed. Two inducible promoters (pTrc and pLux101) were subsequently characterized within the three strains. The inducibility of the pTrc promoter was relatively low across the three strains (induction ratio: 1.98–6.39), whereas the pLux101 promoter demonstrated a significantly greater level of inducibility within the three strains (induction ratio: 87.28–216.71). Finally, through gene knockout experiments, this study identified four genes essential for bacterial cellulose film production in the genome of the Gluconacetobacter hansenii ATCC 5358 strain. This study not only enriches the library of synthetic biology elements in nonmodel strains, but also lays the foundation for the synthetic biology applications of Acetobacteraceae.

    • Public Summary

    • The basic properties of three Acetobacteraceae strains were analyzed.
    • Two inducible promoters were characterized within the three strains, along with the identification of four essential genes for bacterial cellulose production in the Gluconacetobacter hansenii ATCC 5358 strain.

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    • References(51)
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    Figure  1.  Analysis of basic information of three Acetobacteraceae strains. (a) Photograph of the cellulose films produced by the three test strains after 4 d of incubation in 50 mL centrifuge tubes. (b) Dry weights of the cellulose films formed by the three test strains after 4 d of incubation in 12-well plates. The division times (c) and growth curves (d) of the three test strains during static incubation. The growth curves (e) and division times (f) of the three test strains during shaking incubation. The error bars represent the means ± SDs; n = 3, 4; ns = not significant; ** P ≤ 0.01; *** P ≤ 0.001; **** P ≤0.0001(Student’s t test).

    Figure  2.  Plasmid features analysis. (a) Minimum inhibitory concentrations (MICs) of seven antibiotics against the three test strains. R indicates that the test strains can grow in HS broth containing 1200 ng/mL antibiotics; GM, KM, SC, CL, TC, AM, and CM represent gentamicin, kanamycin, spectinomycin, chloramphenicol, tetracycline, ampicillin, and carbenicillin, respectively. Plasmid transformation efficiency (b) and frequency (c) of the three test strains. (d) Enumeration of surviving three test strains on HS agar plates after electroporation. The error bars represent the means ± SDs; n = 3; ns = not significant; *P ≤ 0.05; ** P ≤ 0.01; **** P ≤ 0.0001 (Student’s t test).

    Figure  3.  Plasmid replication and stability analysis. Electropherograms of replicable (a) and stabilizable (b) origins of plasmid replication within the three test strains. M refers to the DNA marker, and R1, V01, C01, P10, and 15a represent the plasmid replication origins pBBR1, pMV01, pSC101, pCrep101, and p15a, respectively. (c) Merged image of the strains in panel a after three months of static culture at room temperature; scale bar, 5 µm.

    Figure  4.  Characterization of the promoter pTrc. (a) Schematic diagram of the engineered strains carrying the pTrc promoter that was tested. Dose response of the inducible promoter pTrc in G. hansenii ATCC 53582 (b), K. rhaeticus iGEM (c) and G. xylinus 700178 (d) to varying IPTG concentrations and RBS intensities after 12 h of induction. (e) Induction curves of the H-trc and H-9trc strains at a 1.0 mM IPTG concentration. (f) Induction curves of the R-trc and R-9trc strains at a 1.0 mM IPTG concentration. (g) Induction curves of the X-trc and X-9trc strains at a 1.0 mM IPTG concentration. (h) OD600 values of strains H-9trc, R-9trc and X-9trc after incubation in HS++ containing different IPTG concentrations for 12 h. (i) The dry weights of BC films from G. hansenii ATCC 53582, K. rhaeticus iGEM, and G. xylinus 700178 incubated in HS++ broth with varying IPTG concentrations. The error bars represent the means ± SDs; n = 3, 4, significant differences among the control group (IPTG concentration of 0 mM) and the other groups were computed via one-way ANOVA; ns = not significant; **** P ≤ 0.0001.

    Figure  5.  Characterization of the promoter pLux101. (a) Dose response of the H-plux, R-plux, and X-plux strains to different concentrations of AHL after 12 h of induction. (b) Induction curves of the H-plux, R-plux, and X-plux strains at a concentration of 500 nM AHL. (c) BC dry weight films from the G. hansenii ATCC 53582, K. rhaeticus iGEM, and G. xylinus 700178 strains after incubation in HS++ broth with varying AHL concentrations for 4 d. (d) OD600 values of H-plux and its correction strains (H-mcs) incubated with various AHL concentrations for 12 h. (e) OD600 values of R-plux and its correction strains (R-mcs) incubated with various AHL concentrations for 12 h. (f) OD600 values of X-plux and its correction strains (wild-type G. xylinus 700178 strain, X-w) incubated with varying AHL concentrations for 12 h. The error bars represent the means ± SEMs; n = 3, 4, significant differences among the control group (AHL concentration of 0 nM) and the other groups were computed via one-way ANOVA; ns = not significant; * P ≤ 0.05, ** P ≤ 0.01, *** P ≤ 0.001 and **** P ≤ 0.0001.

    Figure  6.  Screening of critical genes for bacterial cellulose production. (a) Schematic diagram of pln2 single recombination technology. (b) PCR identification of the nine variant strains obtained via single recombination methods. (c) BC film production of the wild-type G. hansenii ATCC 53582 strain (WT) and nine variant strains after stationary incubation in HS broth. (d) BC film production in 12-well plates of four variant strains after complementation of the corresponding genes.

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    [8]
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    [9]
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    [13]
    Raspor P, Goranovič D. Biotechnological applications of acetic acid bacteria. Critical Reviews in Biotechnology, 2008, 28 (2): 101–124. doi: 10.1080/07388550802046749
    [14]
    Yamashita S, Oe M, Kimura M, et al. Improving effect of acetic acid bacteria ( Gluconacetobacter hansenii GK-1) on sIgA and physical conditions in healthy people: double-blinded placebo-controlled study. Food and Nutrition Sciences, 2022, 13: 541–557. doi: 10.4236/fns.2022.136041
    [15]
    Sengun I Y, Karabiyikli S. Importance of acetic acid bacteria in food industry. Food Control, 2011, 22 (5): 647–656. doi: 10.1016/j.foodcont.2010.11.008
    [16]
    Lynch K M, Zannini E, Wilkinson S, et al. Physiology of acetic acid bacteria and their role in vinegar and fermented beverages. Comprehensive Reviews in Food Science and Food Safety, 2019, 18 (3): 587–625. doi: 10.1111/1541-4337.12440
    [17]
    Moniri M, Boroumand Moghaddam A, Azizi S, et al. Production and status of bacterial cellulose in biomedical engineering. Nanomaterials, 2017, 7 (9): 257. doi: 10.3390/nano7090257
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    [19]
    Srivastava S, Mathur G. Bacterial cellulose: a multipurpose biomaterial for manmade world. Current Applied Science and Technology, 2023, 23 (3): 1–19. doi: 10.55003/cast.2022.03.23.014
    [20]
    Zheng L, Li S S, Luo J W, et al. Latest advances on bacterial cellulose-based antibacterial materials as wound dressings. Frontiers in Bioengineering and Biotechnology, 2020, 8: 593768. doi: 10.3389/fbioe.2020.593768
    [21]
    Gorgieva S, Trček J. Bacterial cellulose: production, modification and perspectives in biomedical applications. Nanomaterials, 2019, 9 (10): 1352. doi: 10.3390/nano9101352
    [22]
    Florea M, Hagemann H, Santosa G, et al. Engineering control of bacterial cellulose production using a genetic toolkit and a new cellulose-producing strain. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113 (24): E3431–E3440. doi: 10.1073/pnas.1522985113
    [23]
    Liu L P, Yang X, Zhao X J, et al. A lambda red and FLP/FRT-mediated site-specific recombination system in Komagataeibacter xylinus and its application to enhance the productivity of bacterial cellulose. ACS Synthetic Biology, 2020, 9 (11): 3171–3180. doi: 10.1021/acssynbio.0c00450
    [24]
    Huang L H, Liu Q J, Sun X W, et al. Tailoring bacterial cellulose structure through CRISPR interference-mediated downregulation of galU in Komagataeibacter xylinus CGMCC 2955. Biotechnology and Bioengineering, 2020, 117 (7): 2165–2176. doi: 10.1002/bit.27351
    [25]
    Jacek P, Kubiak K, Ryngajłło M, et al. Modification of bacterial nanocellulose properties through mutation of motility related genes in Komagataeibacter hansenii ATCC 53582. New Biotechnology, 2019, 52: 60–68. doi: 10.1016/j.nbt.2019.05.004
    [26]
    Battad-Bernardo E, McCrindle S L, Couperwhite I, et al. Insertion of an E. coli lacZ gene in Acetobacter xylinus for the production of cellulose in whey. FEMS Microbiology Letters, 2004, 231 (2): 253–260. doi: 10.1016/S0378-1097(04)00007-2
    [27]
    Hur D H, Choi W S, Kim T Y, et al. Enhanced production of bacterial cellulose in Komagataeibacter xylinus via tuning of biosynthesis genes with synthetic RBS. Journal of Microbiology and Biotechnology, 2020, 30 (9): 1430–1435. doi: 10.4014/jmb.2006.06026
    [28]
    Mangayil R, Rajala S, Pammo A, et al. Engineering and characterization of bacterial nanocellulose films as low cost and flexible sensor material. ACS Applied Materials & Interfaces, 2017, 9 (22): 19048–19056. doi: 10.1021/acsami.7b04927
    [29]
    Fournet-Fayard S, Joly B, Forestier C. Transformation of wild type Klebsiella pneumoniae with plasmid DNA by electroporation. Journal of Microbiological Methods, 1995, 24 (1): 49–54. doi: 10.1016/0167-7012(95)00053-4
    [30]
    Taylor K, Woods S, Johns A, et al. Intrinsic responsible innovation in a synthetic biology research project. New Genetics and Society, 2023, 42 (1): e2232684. doi: 10.1080/14636778.2023.2232684
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