Genetic engineering of low-temperature polyhydroxyalkanoate production by Acidovorax sp. A1169, a psychrophile isolated from a subglacial outflow
Jazyk angličtina Země Německo Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
Grant 2017/24/C/NZ9/00232
Narodowe Centrum Nauki
PubMed
37709928
PubMed Central
PMC10501959
DOI
10.1007/s00792-023-01311-5
PII: 10.1007/s00792-023-01311-5
Knihovny.cz E-zdroje
- Klíčová slova
- Arctic, Bioplastics, Extremophile, Low-temperature biotechnology, Oligotrophy,
- MeSH
- Comamonadaceae * genetika MeSH
- genetické inženýrství MeSH
- polyhydroxyalkanoáty * MeSH
- teplota MeSH
- uhlík MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- polyhydroxyalkanoáty * MeSH
- uhlík MeSH
In recent years, extremophilic microorganisms have been employed as producers of the microbial bioplastics polyhydroxyalkanoates (PHA), which are of great biotechnological value. Nevertheless, cold-loving or psychrophilic (cryophilic) bacteria have been neglected in this regard. Here, we present an investigation of the Arctic glacier-derived PHA producer Acidovorax sp. A1169. Biolog GEN III Microplates were used as a screening tool to identify the most suitable carbon substrate concerning PHA synthesis. The strain produced homopolymer poly(3-hydroxybutyrate) (PHB) most efficiently (2 g/L) at a temperature of 15 °C when supplied with fructose or mannitol as carbon sources with a substantial decrease of PHB biosynthesis at 17.5 °C. The PHB yield did not increase considerably or even decreased when carbon source concentration exceeded 10 g/L hinting that the strain is oligotrophic in nature. The strain was also capable of introducing 3-hydroxyvalerate (3HV) into the polymer structure, which is known to improve PHA thermoplastic properties. This is the first investigation providing insight into a PHA biosynthesis process by means of a true psychrophile, offering guidelines on polar-region bacteria cultivation, production of PHA and also on the methodology for genetic engineering of psychrophiles.
Zobrazit více v PubMed
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. https://www.bioinformatics.babraham.ac.uk/projects/fastqc
Aramvash A, Akbari Shahabi Z, Dashti Aghjeh S, Ghafari MD. Statistical physical and nutrient optimization of bioplastic polyhydroxybutyrate production by Cupriavidus necator. Int J Environ Sci Technol. 2015;12:2307–2316. doi: 10.1007/s13762-015-0768-3. DOI
Azevedo NF, Bragança SM, Simões LC, Cerqueira L, Almeida C, Keevil CW, Vieira MJ. Proposal for a method to estimate nutrient shock effects in bacteria. BMC Res Notes. 2012;5(1):1–6. doi: 10.1186/1756-0500-5-422. PubMed DOI PMC
Belal EB. Production of poly-β-hydroxybutyric acid (PHB) by Rhizobium elti and Pseudomonas stutzeri. Curr Res J Biol. 2013;5(6):273–284. doi: 10.19026/crjbs.5.5429. DOI
Cerrone F, Davis R, Kenny ST, Woods T, O’Donovan A, Gupta VK, et al. Use of a mannitol rich ensiled grass press juice (EGPJ) as a sole carbon source for polyhydroxyalkanoates (PHAs) production through high cell density cultivation. Bioresour Technol. 2015;191:45–52. doi: 10.1016/j.biortech.2015.04.128. PubMed DOI
Chen GQ, Jiang XR. Next generation industrial biotechnology based on extremophilic bacteria. Curr Opin Biotechnol. 2018;50:94–100. doi: 10.1016/j.copbio.2017.11.016. PubMed DOI
Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34(17):i884–i890. doi: 10.1093/bioinformatics/bty560. PubMed DOI PMC
Choi TR, Park YL, Song HS, Lee SM, Park SL, Lee HS, et al. Fructose-based production of short-chain-length and medium-chain-length polyhydroxyalkanoate copolymer by arctic Pseudomonas sp. B14–6. Polymers. 2021;13(9):1398. doi: 10.3390/polym13091398. PubMed DOI PMC
Ciesielski S, Górniak D, Możejko J, Świątecki A, Grzesiak J, Zdanowski M. The diversity of bacteria isolated from Antarctic freshwater reservoirs possessing the ability to produce polyhydroxyalkanoates. Curr Microbiol. 2014;69:594–603. doi: 10.1007/s00284-014-0629-1. PubMed DOI PMC
Corrado I, Petrillo C, Isticato R, Casillo A, Corsaro MM, Sannia G, Pezzella C. The power of two: an artificial microbial consortium for the conversion of inulin into polyhydroxyalkanoates. Int J Biol Macromol. 2021;189:494–502. doi: 10.1016/j.ijbiomac.2021.08.123. PubMed DOI
DeAngelis KM, D’Haeseleer P, Chivian D, Fortney JL, Khudyakov J, Simmons B, et al. Complete genome sequence of “Enterobacter lignolyticus” SCF1. Stand Genom Sci. 2011;5(1):69–85. doi: 10.4056/sigs.2104875. PubMed DOI PMC
Du J, Liu Y, Zhu H. Genome-based analyses of the genus Acidovorax: proposal of the two novel genera Paracidovorax gen. nov., Paenacidovorax gen. nov. and the reclassification of Acidovorax antarcticus as Comamonas antarctica comb. nov. and emended description of the genus Acidovorax. Arch Microbiol. 2023;205(1):1–10. doi: 10.1007/s00203-022-03379-7. PubMed DOI
El-Sayed AK, Hothersall J, Thomas CM. Quorum-sensing-dependent regulation of biosynthesis of the polyketide antibiotic mupirocin in Pseudomonas fluorescens NCIMB 10586. Microbiology. 2001;147(8):2127–2139. doi: 10.1099/00221287-147-8-2127. PubMed DOI
Gawor J, Grzesiak J, Sasin-Kurowska J, Borsuk P, Gromadka R, Górniak D, et al. Evidence of adaptation, niche separation and microevolution within the genus Polaromonas on Arctic and Antarctic glacial surfaces. Extremophiles. 2016;20:403–413. doi: 10.1007/s00792-016-0831-0. PubMed DOI PMC
Georlette D, Blaise V, Collins T, D'Amico S, Gratia E, Hoyoux A, et al. Some like it cold: biocatalysis at low temperatures. FEMS Microbiol Rev. 2004;28(1):25–42. doi: 10.1016/j.femsre.2003.07.003. PubMed DOI
Gnaim R, Unis R, Gnayem N, Das J, Gozin M, Golberg A. Turning mannitol-rich agricultural waste to poly(3-hydroxybutyrate) with Cobetia amphilecti fermentation and recovery with methyl levulinate as a green solvent. Bioresour Technol. 2022;352:127075. doi: 10.1016/j.biortech.2022.127075. PubMed DOI
Goh YS, Tan IKP. Polyhydroxyalkanoate production by Antarctic soil bacteria isolated from Casey Station and Signy Island. Microbiol Res. 2012;167(4):211–219. doi: 10.1016/j.micres.2011.08.002. PubMed DOI
Grzesiak J, Górniak D, Świątecki A, Aleksandrzak-Piekarczyk T, Szatraj K, Zdanowski MK. Microbial community development on the surface of Hans and Werenskiold Glaciers (Svalbard, Arctic): a comparison. Extremophiles. 2015;19:885–897. doi: 10.1007/s00792-015-0764-z. PubMed DOI PMC
Handrick R, Reinhardt S, Jendrossek D. Mobilization of poly (3-hydroxybutyrate) in Ralstonia eutropha. J Bacteriol. 2000;182(20):5916–5918. doi: 10.1128/jb.182.20.5916-5918.2000. PubMed DOI PMC
Hong JW, Song HS, Moon YM, Hong YG, Bhatia SK, Jung HR, et al. Polyhydroxybutyrate production in halophilic marine bacteria Vibrio proteolyticus isolated from the Korean peninsula. Bioprocess Biosyst Eng. 2019;42:603–610. doi: 10.1007/s00449-018-02066-6. PubMed DOI
Inoue H, Nojima H, Okayama H. High efficiency transformation of Escherichia coli with plasmids. Gene. 1990;96(1):23–28. doi: 10.1016/0378-1119(90)90336-p. PubMed DOI
Kadouri D, Jurkevitch E, Okon Y. Poly β-hydroxybutyrate depolymerase (PhaZ) in Azospirillum brasilense and characterization of a phaZ mutant. Arch Microbiol. 2003;180:309–318. doi: 10.1007/s00203-003-0590-z. PubMed DOI
Kessler B, Witholt B. Factors involved in the regulatory network of polyhydroxyalkanoate metabolism. J Biotechnol. 2001;86(2):97–104. doi: 10.1016/s0168-1656(00)00404-1. PubMed DOI
Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol. 2014;64(2):346–351. doi: 10.1099/ijs.0.059774-0. PubMed DOI
Knoll M, Hamm TM, Wagner F, Martinez V, Pleiss J. The PHA depolymerase engineering database: a systematic analysis tool for the diverse family of polyhydroxyalkanoate (PHA) depolymerases. BMC Bioinform. 2009;10:1–8. doi: 10.1186/1471-2105-10-89. PubMed DOI PMC
Koller M. Production of polyhydroxyalkanoate (PHA) biopolyesters by extremophiles. MOJ Polym Sci. 2017;1(2):1–19. doi: 10.15406/mojps.2017.01.00011. DOI
Koller M. Chemical and biochemical engineering approaches in manufacturing polyhydroxyalkanoate (PHA) biopolyesters of tailored structure with focus on the diversity of building blocks. Chem Biochem Eng Q. 2018;32(4):413–438. doi: 10.15255/CABEQ.2018.1385. DOI
Koller M, Salerno A, Dias M, Reiterer A, Braunegg G. Modern biotechnological polymer synthesis: a review. Food Technol Biotechnol. 2010;48(3):255–269.
Koller M, Maršálek L, de Sousa Dias MM, Braunegg G. Producing microbial polyhydroxyalkanoate (PHA) biopolyesters in a sustainable manner. Nat Biotechnol. 2017;37:24–38. doi: 10.1016/j.nbt.2016.05.001. PubMed DOI
Kourilova X, Pernicova I, Sedlar K, Musilova J, Sedlacek P, Kalina M, et al. Production of polyhydroxyalkanoates (PHA) by a thermophilic strain of Schlegelella thermodepolymerans from xylose rich substrates. Bioresour Technol. 2020;315:123885. doi: 10.1016/j.biortech.2020.123885. PubMed DOI
Kourilova X, Pernicova I, Vidlakova M, Krejcirik R, Mrazova K, Hrubanova K, et al. Biotechnological conversion of grape pomace to poly(3-hydroxybutyrate) by moderately thermophilic bacterium Tepidimonas taiwanensis. Bioengineering. 2021;8(10):141. doi: 10.3390/bioengineering8100141. PubMed DOI PMC
Kouřilová X, Schwarzerová J, Pernicová I, Sedlář K, Mrázová K, Krzyžánek V, et al. The first insight into polyhydroxyalkanoates accumulation in multi-extremophilic Rubrobacter xylanophilus and Rubrobacter spartanus. Microorganisms. 2021;9(5):909. doi: 10.3390/microorganisms9050909. PubMed DOI PMC
Kumar V, Thakur V, Kumar V, Kumar R, Singh D. Genomic insights revealed physiological diversity and industrial potential for Glaciimonas sp. PCH181 isolated from Satrundi glacier in Pangi-Chamba Himalaya. Genomics. 2020;112(1):637–646. doi: 10.1016/j.ygeno.2019.04.016. PubMed DOI
Kumar V, Thakur V, Ambika, Kumar S, Singh D (2018) Bioplastic reservoir of diverse bacterial communities revealed along altitude gradient of Pangi-Chamba trans-Himalayan region. FEMS Microbiol Lett 365(14):fny144 PubMed
Madigan MT, Bender KS, Buckley DH, Sattley WM, Stahl DA. Brock biology of microorganisms. Boston, US: Benjamin Cummins; 2019. pp. 1391–1407.
Margesin R, Schinner F, Marx JC, Gerday C. Psychrophiles: from biodiversity to biotechnology. Berlin: Springer; 2008. pp. 1–462.
Mezzina MP, Pettinari MJ. Phasins, multifaceted polyhydroxyalkanoate granule-associated proteins. Appl Environ Microbiol. 2016;82(17):5060–5067. doi: 10.1128/AEM.01161-16. PubMed DOI PMC
Mohr PW, Krawiec S. Temperature characteristics and Arrhenius plots for nominal psychrophiles, mesophiles and thermophiles. Microbiology. 1980;121(2):311–317. doi: 10.1099/00221287-121-2-311. PubMed DOI
Moradali MF, Rehm BH. Bacterial biopolymers: from pathogenesis to advanced materials. Nat Rev Microbiol. 2020;18(4):195–210. doi: 10.1038/s41579-019-0313-3. PubMed DOI PMC
Mostafa YS, Alrumman SA, Otaif KA, Alamri SA, Mostafa MS, Sahlabji T. Production and characterization of bioplastic by polyhydroxybutyrate accumulating Erythrobacter aquimaris isolated from mangrove rhizosphere. Molecules. 2020;25(1):179. doi: 10.3390/molecules25010179. PubMed DOI PMC
Możejko-Ciesielska J, Kiewisz R. Bacterial polyhydroxyalkanoates: still fabulous? Microbiol Res. 2016;192:271–282. doi: 10.1016/j.micres.2016.07.010. PubMed DOI
Müller-Santos M, Koskimäki JJ, Alves LPS, de Souza EM, Jendrossek D, Pirttilä AM. The protective role of PHB and its degradation products against stress situations in bacteria. FEMS Microbiol Rev. 2021;45(3):fuaa058. doi: 10.1093/femsre/fuaa058. PubMed DOI
Nowroth V, Marquart L, Jendrossek D. Low temperature-induced viable but not culturable state of Ralstonia eutropha and its relationship to accumulated polyhydroxybutyrate. Microbiol Lett. 2016;363(23):fnw249. doi: 10.1093/femsle/fnw249. PubMed DOI PMC
Nygaard D, Yashchuk O, Noseda DG, Araoz B, Hermida ÉB. Improved fermentation strategies in a bioreactor for enhancing poly(3-hydroxybutyrate)(PHB) production by wild type Cupriavidus necator from fructose. Heliyon. 2021;7(1):e05979. doi: 10.1016/j.heliyon.2021.e05979. PubMed DOI PMC
Obruca S, Snajdar O, Svoboda Z, Marova I. Application of random mutagenesis to enhance the production of polyhydroxyalkanoates by Cupriavidus necator H16 on waste frying oil. World J Microbiol Biotechnol. 2013;29:2417–2428. doi: 10.1007/s11274-013-1410-5. PubMed DOI
Obruca S, Sedlacek P, Krzyzanek V, Mravec F, Hrubanova K, Samek O, et al. Accumulation of poly (3-hydroxybutyrate) helps bacterial cells to survive freezing. PLoS ONE. 2016;11(6):e0157778. doi: 10.1371/journal.pone.0157778. PubMed DOI PMC
Pacheco N, Orellana-Saez M, Pepczynska M, Enrione J, Bassas-Galia M, Borrero-de Acuña JM, et al. Exploiting the natural poly (3-hydroxyalkanoates) production capacity of Antarctic Pseudomonas strains: from unique phenotypes to novel biopolymers. J Ind Microbiol Biotechnol. 2019;46(8):1139–1153. doi: 10.1007/s10295-019-02186-2. PubMed DOI
Park YL, Bhatia SK, Gurav R, Choi TR, Kim HJ, Song HS, et al. Fructose based hyper production of poly-3-hydroxybutyrate from Halomonas sp. YLGW01 and impact of carbon sources on bacteria morphologies. Int J Biol Macromol. 2020;154:929–936. doi: 10.1016/j.ijbiomac.2020.03.129. PubMed DOI
Reddy CSK, Ghai R, Kalia V. Polyhydroxyalkanoates: an overview. Biores Technol. 2003;87(2):137–146. doi: 10.1016/S0960-8524(02)00212-2. PubMed DOI
Rehakova V, Pernicova I, Kourilova X, Sedlacek P, Musilova J, Sedlar K, et al. Biosynthesis of versatile PHA copolymers by thermophilic members of the genus Aneurinibacillus. Int J Biol Macromol. 2023;225:1588–1598. doi: 10.1016/j.ijbiomac.2022.11.215. PubMed DOI
Rogala MM, Gawor J, Gromadka R, Kowalczyk M, Grzesiak J. Biodiversity and habitats of polar region polyhydroxyalkanoic acid-producing bacteria: bioprospection by popular screening methods. Genes. 2020;11(8):873. doi: 10.3390/genes11080873. PubMed DOI PMC
Sandle T, Skinner K, Sandle J, Gebala B, Kothandaraman P. Evaluation of the GEN III OmniLog® ID System microbial identification system for the profiling of cleanroom bacteria. Eur J Parenter Pharm Sci. 2013;18(2):44–50.
Smorawinska M, Szuplewska M, Zaleski P, Wawrzyniak P, Maj A, Plucienniczak A, Bartosik D. Mobilizable narrow host range plasmids as natural suicide vectors enabling horizontal gene transfer among distantly related bacterial species. FEMS Microbiol Lett. 2012;326(1):76–82. doi: 10.1111/j.1574-6968.2011.02432.x. PubMed DOI
Sriyapai T, Chuarung T, Kimbara K, Samosorn S, Sriyapai P. Production and optimization of polyhydroxyalkanoates (PHAs) from Paraburkholderia sp. PFN 29 under submerged fermentation. Electron J Biotechnol. 2022;56:1–11. doi: 10.1016/j.ejbt.2021.12.003. DOI
Tan D, Wang Y, Tong Y, Chen GQ. Grand challenges for industrializing polyhydroxyalkanoates (PHAs) Trends Biotechnol. 2021;39(9):953–963. doi: 10.1016/j.tibtech.2020.11.010. PubMed DOI
Tripathi AD, Yadav A, Jha A, Srivastava SK. Utilizing of sugar refinery waste (cane molasses) for production of bio-plastic under submerged fermentation process. J Polym Environ. 2012;20:446–453. doi: 10.1007/s10924-011-0394-1. DOI
Tripathi AD, Srivastava SK, Singh RP. Statistical optimization of physical process variables for bio-plastic (PHB) production by Alcaligenes sp. Biomass Bioenergy. 2013;55:243–250. doi: 10.1016/j.biombioe.2013.02.017. DOI
Wang Z, Zheng Y, Ji M, Zhang X, Wang H, Chen Y, et al. Hyperproduction of PHA copolymers containing high fractions of 4-hydroxybutyrate (4HB) by outer membrane-defected Halomonas bluephagenesis grown in bioreactors. Microb Biotechnol. 2022;15(5):1586–1597. doi: 10.1111/1751-7915.13999. PubMed DOI PMC
Wang J, Liu S, Huang J, Cui R, Xu Y, Song Z. Genetic engineering strategies for sustainable polyhydroxyalkanoate (PHA) production from carbon-rich wastes. Environ Technol Innov. 2023;30:103069. doi: 10.1016/j.eti.2023.103069. DOI
Weimer A, Kohlstedt M, Volke DC, Nikel PI, Wittmann C. Industrial biotechnology of Pseudomonas putida: advances and prospects. Appl Microbiol Biotechnol. 2020;104:7745–7766. doi: 10.1007/s00253-020-10811-9. PubMed DOI PMC
Wendy YD, Fauziah MN, Baidurah YS, Tong WY, Lee CK. Production and characterization of polyhydroxybutyrate (PHB) by Burkholderia cepacia BPT1213 using waste glycerol as carbon source. Biocatal Agric Biotechnol. 2022;41:102310. doi: 10.1016/j.bcab.2022.102310. DOI
Willems A. The family Comamonadaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The prokaryotes: Alphaproteobacteria and Betaproteobacteria. 4. Berlin: Springer; 2014. pp. 777–851.
Wilson K. Preparation of genomic DNA from bacteria. Curr Protoc Mol Biol. 2001;56(1):2–4. PubMed
Wolfenden R, Yuan Y. Rates of spontaneous cleavage of glucose, fructose, sucrose, and trehalose in water and the catalytic proficiencies of invertase and trehalase. J Am Chem Soc. 2008;130(24):7548–7549. doi: 10.1021/ja802206s. PubMed DOI PMC
Woźniak M, Gałązka A, Tyśkiewicz R, Jaroszuk-Ściseł J. Endophytic bacteria potentially promote plant growth by synthesizing different metabolites and their phenotypic/physiological profiles in the Biolog GEN III MicroPlateTM Test. Int J Mol Sci. 2019;20(21):5283. doi: 10.3390/ijms20215283. PubMed DOI PMC
Yamaguchi T, Narsico J, Kobayashi T, Inoue A, Ojima T. Production of poly(3-hydroyxybutyrate) by a novel alginolytic bacterium Hydrogenophaga sp. strain UMI-18 using alginate as a sole carbon source. J Biosci Bioeng. 2019;128(2):203–208. doi: 10.1016/j.jbiosc.2019.02.008. PubMed DOI
Zhang L, Jiang Z, Tsui TH, Loh KC, Dai Y, Tong YW. A review on enhancing Cupriavidus necator fermentation for poly(3-hydroxybutyrate)(PHB) production from low-cost carbon sources. Front Bioeng Biotechnol. 2022;10:946085. doi: 10.3389/fbioe.2022.946085. PubMed DOI PMC