Chemoautotrophic production of gaseous hydrocarbons, bioplastics and osmolytes by a novel Halomonas species.


Journal

Biotechnology for biofuels and bioproducts
ISSN: 2731-3654
Titre abrégé: Biotechnol Biofuels Bioprod
Pays: England
ID NLM: 9918300888906676

Informations de publication

Date de publication:
11 Oct 2023
Historique:
received: 09 08 2023
accepted: 25 09 2023
medline: 12 10 2023
pubmed: 12 10 2023
entrez: 11 10 2023
Statut: epublish

Résumé

Production of relatively low value, bulk commodity chemicals and fuels by microbial species requires a step-change in approach to decrease the capital and operational costs associated with scaled fermentation. The utilisation of the robust and halophilic industrial host organisms of the genus Halomonas could dramatically decrease biomanufacturing costs owing to their ability to grow in seawater, using waste biogenic feedstocks, under non-sterile conditions. We describe the isolation of Halomonas rowanensis, a novel facultative chemoautotrophic species of Halomonas from a natural brine spring. We investigated the ability of this species to produce ectoine, a compound of considerable industrial interest, under heterotrophic conditions. Fixation of radiolabelled NaH This proof-of-concept study illustrates the value of recruiting environmental isolates as industrial hosts for chemicals biomanufacturing, where CO

Sections du résumé

BACKGROUND BACKGROUND
Production of relatively low value, bulk commodity chemicals and fuels by microbial species requires a step-change in approach to decrease the capital and operational costs associated with scaled fermentation. The utilisation of the robust and halophilic industrial host organisms of the genus Halomonas could dramatically decrease biomanufacturing costs owing to their ability to grow in seawater, using waste biogenic feedstocks, under non-sterile conditions.
RESULTS RESULTS
We describe the isolation of Halomonas rowanensis, a novel facultative chemoautotrophic species of Halomonas from a natural brine spring. We investigated the ability of this species to produce ectoine, a compound of considerable industrial interest, under heterotrophic conditions. Fixation of radiolabelled NaH
CONCLUSIONS CONCLUSIONS
This proof-of-concept study illustrates the value of recruiting environmental isolates as industrial hosts for chemicals biomanufacturing, where CO

Identifiants

pubmed: 37821908
doi: 10.1186/s13068-023-02404-1
pii: 10.1186/s13068-023-02404-1
pmc: PMC10568851
doi:

Types de publication

Journal Article

Langues

eng

Pagination

152

Subventions

Organisme : Engineering and Physical Sciences Research Council (EPSRC) and Biotechnology and Biological Sciences Research Council (BBSRC)
ID : EP/S01778X/1
Organisme : Engineering and Physical Sciences Research Council (EPSRC) and Biotechnology and Biological Sciences Research Council (BBSRC)
ID : EP/S01778X/1
Organisme : Engineering and Physical Sciences Research Council (EPSRC) and Biotechnology and Biological Sciences Research Council (BBSRC)
ID : EP/S01778X/1
Organisme : Engineering and Physical Sciences Research Council (EPSRC) and Biotechnology and Biological Sciences Research Council (BBSRC)
ID : EP/S01778X/1
Organisme : Engineering and Physical Sciences Research Council (EPSRC) and Biotechnology and Biological Sciences Research Council (BBSRC)
ID : EP/S01778X/1

Informations de copyright

© 2023. BioMed Central Ltd., part of Springer Nature.

Références

Yan Q, Pfleger BF. Revisiting metabolic engineering strategies for microbial synthesis of oleochemicals. Metab Eng. 2020;58:35–46.
pubmed: 31022535
Amer M, Wojcik EZ, Sun C, Hoeven R, Hughes JMX, Faulkner M, et al. Low carbon strategies for sustainable bio-alkane gas production and renewable energy. Energy Environ Sci. 2020;13:1818–31.
Liu X, Miao R, Lindberg P, Lindblad P. Modular engineering for efficient photosynthetic biosynthesis of 1-butanol from CO
Webb JP, Arnold SA, Baxter S, Hall SJ, Eastham G, Stephens G. Efficient bio-production of citramalate using an engineered Escherichia coli strain. Microbiology. 2017;164:133–41.
pubmed: 29231156 pmcid: 5882075
Xiao-Ran J, Jin Y, Xiangbin C, Guo-Qiang C. Halomonas and pathway engineering for bioplastics production. Meth Enzymol. 2018;608:309–28.
Wu W, Maravelias CT. Synthesis and techno-economic assessment of microbial-based processes for terpenes production. Biotechnol Biofuels. 2018;11:294.
pubmed: 30386431 pmcid: 6203976
Chen G-Q, Jiang X-R. Next generation industrial biotechnology based on extremophilic bacteria. Curr Opin Biotechnol. 2018;50:94–100.
pubmed: 29223022
Fujiwara S. Extremophiles: developments of their special functions and potential resources. J Biosci Bioeng. 2002;94:518–25.
pubmed: 16233344
Merino N, Aronson HS, Bojanova DP, Feyhl-Buska J, Wong ML, Zhang S, et al. Living at the extremes: extremophiles and the limits of life in a planetary context. Front Microbiol. 2019;10:780.
pubmed: 31037068 pmcid: 6476344
Sayed AM, Hassan MHA, Alhadrami HA, Hassan HM, Goodfellow M, Rateb ME. Extreme environments: microbiology leading to specialised metabolites. J Appl Microbiol. 2020;128:630–57.
pubmed: 31310419
Zhang X, Lin Y, Chen G-Q. Halophiles as chassis for bioproduction. Adv Biosyst. 2018;2:1800088.
Tao W, Lv L, Chen G-Q. Engineering Halomonas species TD01 for enhanced polyhydroxyalkanoates synthesis via CRISPRi. Microb Cell Fact. 2017;16:48.
pubmed: 28381263 pmcid: 5382479
Ye J, Huang W, Wang D, Chen F, Yin J, Li T, et al. Pilot scale-up of poly(3-hydroxybutyrate-co-4-hydroxybutyrate) production by Halomonas bluephagenesis via cell growth adapted optimization process. Biotechnol J. 2018;13:1800074.
Oren A. Industrial and environmental applications of halophilic microorganisms. Environ Technol. 2010;31:825–34.
pubmed: 20662374
Chen Y-H, Lu C-W, Shyu Y-T, Lin S-S. Revealing the saline adaptation strategies of the halophilic bacterium Halomonas beimenensis through high-throughput omics and transposon mutagenesis approaches. Sci Rep. 2017;7:13037.
pubmed: 29026163 pmcid: 5638851
Fu X-Z, Tan D, Aibaidula G, Wu Q, Chen J-C, Chen G-Q. Development of Halomonas TD01 as a host for open production of chemicals. Metab Eng. 2014;23:78–91.
pubmed: 24566041
Trisrivirat D, Hughes JMX, Hoeven R, Faulkner M, Toogood H, Chaiyen P, et al. Promoter engineering for microbial bio-alkane gas production. Synth Biol. 2020;5:ysaa022.
Zhao H, Zhang HM, Chen X, Li T, Wu Q, Ouyang Q, et al. Novel T7-like expression systems used for Halomonas. Metab Eng. 2017;39:128–40.
pubmed: 27889295
Li T, Elhadi D, Chen G-Q. Co-production of microbial polyhydroxyalkanoates with other chemicals. Metab Eng. 2017;43:29–36.
pubmed: 28782693
Amer M, Hoeven R, Kelly P, Faulkner M, Smith MH, Toogood HS, et al. Renewable and tuneable bio-LPG blends derived from amino acids. Biotechnol Biofuels. 2020;13:125.
pubmed: 32684978 pmcid: 7362463
Mishra S, Raghuvanshi S, Gupta S, Raj K. Application of novel thermo-tolerant haloalkalophilic bacterium Halomonas stevensii for bio mitigation of gaseous phase CO
Simon R, Priefer U, Puhler A. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Technology. 1983;1:784–91.
Tan D, Xue Y-S, Aibaidula G, Chen G-Q. Unsterile and continuous production of polyhydroxybutyrate by Halomonas TD01. Bioresour Technol. 2011;102:8130–6.
pubmed: 21680179
Janda JM, Abbott SL. 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J Clin Microbiol. 2007;45:2761–4.
pubmed: 17626177 pmcid: 2045242
Carver T, Harris SR, Berriman M, Parkhill J, McQuillan JA. Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics. 2012;28:464–9.
pubmed: 22199388
Davis JJ, Wattam AR, Aziz RK, Brettin T, Butler R, Butler RM, et al. The PATRIC bioinformatics resource center: expanding data and analysis capabilities. Nucleic Acids Res. 2020;48:D606–12.
pubmed: 31667520
Felsenstein J. PHYLIP–Phylogeny Inference Package (Version 3.2). Cladistics. 1989;5:164–6.
Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, et al. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 2019;47:W636–41.
pubmed: 30976793 pmcid: 6602479
Lim A, Zhang L. WebPHYLIP: a web interface to PHYLIP. Bioinformatics. 1999;15:1068–9.
pubmed: 10746002
Huerta-Cepas J, Serram F, Bork P. ETE 3: Reconstruction, analysis and visualization of phylogenomic data. Mol Biol Evol. 2016;33:1635–8.
pubmed: 26921390 pmcid: 4868116
Karp PD, Midford PE, Billington R, Kothari A, Krummenacker M, Latendresse M, et al. Pathway tools version 23.0 update: software for pathway/genome informatics and systems biology. Brief Bioinform. 2021;22:109–26.
pubmed: 31813964
Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596:583–9.
pubmed: 34265844 pmcid: 8371605
Schrödinger L, DeLano W. PyMOL. In. 2020.
Holm L. DALI and the persistence of protein shape. Protein Sci. 2020;29:128–40.
pubmed: 31606894
Sauer T, Galinski EA. Bacterial milking: a novel bioprocess for production of compatible solutes. Biotechnol Bioeng. 1998;59:128.
pubmed: 10099323
Park H, Toogood HS, Chen G-Q, Scrutton NS. Co-production of biofuel, bioplastics, and biochemicals during extended fermentation of Halomonas bluephagenesis. Microb Biotechnol. 2022;16:307–21.
pubmed: 36353812 pmcid: 9871518
Sun Y, Casella S, Fang Y, Huang F, Faulkner M, Barrett S, et al. Light modulates the biosynthesis and organization of cyanobacterial carbon fixation machinery through photosynthetic electron flow. Plant Physiol. 2016;171:530–41.
pubmed: 26956667 pmcid: 4854705
Lee JC, Jeon CO, Lim JM, Lee SM, Lee JM, Song SM, et al. Halomonas taeanensis sp. Nov., a novel moderately halophilic bacterium isolated from a solar saltern in Korea. Int J Syst Evol Microbiol. 2005;55:2027–32.
pubmed: 16166705
Nakayama H, Yoshida K, Ono H, Murooka Y, Shinmyo A. Ectoine, the compatible solute of Halomonas elongata, confers hyperosmotic tolerance in cultured tobacco cells. Plant Physiol. 2000;122:1239–47.
pubmed: 10759521 pmcid: 58960
Liu M, Liu H, Shi M, Jiang M, Li L, Zheng Y. Microbial production of ectoine and hydroxyectoine as high-value chemicals. Microb Cell Fact. 2021;20:76.
pubmed: 33771157 pmcid: 7995798
Grammann K, Volke A, Kunte HJ. New type of osmoregulated solute transporter identified in halophilic members of the bacteria domain: TRAP transporter teaABC mediates uptake of ectoine and hydroxyectoine in Halomonas elongata DSM 2581T. J Bacteriol. 2002;184:3078–85.
pubmed: 12003950 pmcid: 135061
Medupin C, Bark R, Owusu K. Land cover and water quality patterns in an urban river: a case study of river Medlock, Greater Manchester. UK Water. 2020;12:848.
Faulkner M, Rodriguez-Ramos J, Dykes GF, Owen SV, Casella S, Simpson DM, et al. Direct characterization of the native structure and mechanics of cyanobacterial carboxysomes. Nanoscale. 2017;9:10662–73.
pubmed: 28616951 pmcid: 5708340
Jurtshuk PJ. Bacterial Metabolism. In: S B, editors. Medical Microbiology. Galveston, Texas: University of Texas Medical Branch at Galveston. 1996.
Dou Z, Heinhorst S, Williams EB, Murin CD, Shively JM, Cannon GC. CO
pubmed: 18258595
Badger MR, Price GD. CO
pubmed: 12554704
Nunoura T, Chikaraishi Y, Izaki R, Suwa T, Sato T, Harada T, et al. A primordial and reversible TCA cycle in a facultatively chemolithoautotrophic thermophile. Science. 2018;359:559–63.
pubmed: 29420286
Campbell BJ, Cary SC. Abundance of reverse tricarboxylic acid cycle genes in free-living microorganisms at deep-sea hydrothermal vents. Appl Environ Microbiol. 2004;70:6282–9.
pubmed: 15466576 pmcid: 522104
Huber H, Gallenberger M, Jahn U, Eylert E, Berg IA, Kockelkorn D, et al. A dicarboxylate/4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic Archaeum Ignicoccus hospitalis. Proc Natl Acad Sci USA. 2008;105:7851–6.
pubmed: 18511565 pmcid: 2409403
Hügler M, Fuchs G. Assaying for the 3-hydroxypropionate cycle of carbon fixation. Methods Enzymol. 2005;397:212–21.
pubmed: 16260293
Leung IK, Krojer TJ, Kochan GT, Henry L, von Delft F, Claridge TD, et al. Structural and mechanistic studies on γ-butyrobetaine hydroxylase. Chem Biol. 2010;17:1316–24.
pubmed: 21168767
Amend JP, Rogers KL, Shock EL, Gurrieri S, Inguaggiato S. Energetics of chemolithoautotrophy in the hydrothermal system of Vulcano Island, southern Italy. Geobiology. 2003;1:37–58.
Veith A, Botelho HM, Kindinger F, Gomes CM, Kletzin A. The sulfur oxygenase reductase from the mesophilic bacterium Halothiobacillus neapolitanus is a highly active thermozyme. J Bacteriol. 2012;194:677–85.
pubmed: 22139503 pmcid: 3264067
Whaley-Martin K, Jessen GL, Nelson TC, Mori JF, Apte S, Jarolimek C, et al. The potential role of Halothiobacillus spp. in sulfur oxidation and acid generation in circum-neutral mine tailings reservoirs. Front Microbiol. 2019;10:297.
pubmed: 30906283 pmcid: 6418380
Kurth JM, Brito JA, Reuter J, Flegler A, Koch T, Franke T, et al. Electron accepting units of the diheme cytochrome c TsdA, a bifunctional thiosulfate dehydrogenase/tetrathionate reductase. J Biol Chem. 2016;291:24804–18.
pubmed: 27694441 pmcid: 5122753
Ray WK, Zeng G, Potters MB, Mansuri AM, Larson TJ. Characterization of a 12-kilodalton rhodanese encoded by glpE of Escherichia coli and its interaction with thioredoxin. J Bacteriol. 2000;182:2277–84.
pubmed: 10735872 pmcid: 111278
Agren D, Schnell R, Oehlmann W, Singh M, Schneider G. Cysteine synthase (CysM) of Mycobacterium tuberculosis is an O-phosphoserine sulfhydrylase: evidence for an alternative cysteine biosynthesis pathway in mycobacteria. J Biol Chem. 2008;283:31567–74.
pubmed: 18799456
Sorigué D, Légeret B, Cuiné S, Blangy S, Moulin S, Billon E, et al. An algal photoenzyme converts fatty acids to hydrocarbons. Science. 2017;357:903–7.
pubmed: 28860382
Zhang L, Liang Y, Wu W, Tan X, Lu X. Microbial synthesis of propane by engineering valine pathway and aldehyde-deformylating oxygenase. Biotechnol Biofuels. 2016;9:80.
pubmed: 27042209 pmcid: 4818529
Natarajan KA. Biotechnology for gold mining, extraction, and waste control. In: Natarajan KA, editor. Biotechnology of Metals. Amsterdam: Elsevier; 2018. p. 179–210.
Vachon DT, Schmidtke NW. Steel industry wastes. J Water Pollut Control Feder. 1981;53:844–7.
Stuber HA, Leenheer JA, Farrier DS. Inorganic sulfur species in waste waters from in situ oil shale processing. J Environ Sci Health Part A Environ Sci Eng. 1978;13:663–75.
Oh S-R, Kim J-K, Lee M-J, Choi K. Dechlorination with sodium thiosulfate affects the toxicity of wastewater contaminated with copper, cadmium, nickel, or zinc. Environ Toxicol. 2008;23:211–7.
pubmed: 18214916

Auteurs

Matthew Faulkner (M)

Manchester Institute of Biotechnology, The University of Manchester, 131 Princess Street, Manchester, M1 7DN, UK.

Robin Hoeven (R)

C3 Biotechnologies Ltd, 20 Mannin Way, Caton Road, Lancaster, LA1 35W, Lancashire, UK.
Engineering Building A, University of Manchester, Oxford Road, Manchester, M13 9PL, UK.

Paul P Kelly (PP)

Manchester Institute of Biotechnology, The University of Manchester, 131 Princess Street, Manchester, M1 7DN, UK.

Yaqi Sun (Y)

Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Biosciences Building, Crown Street, Liverpool, L69 7BE, UK.

Helen Park (H)

Manchester Institute of Biotechnology, The University of Manchester, 131 Princess Street, Manchester, M1 7DN, UK.

Lu-Ning Liu (LN)

Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Biosciences Building, Crown Street, Liverpool, L69 7BE, UK.

Helen S Toogood (HS)

Manchester Institute of Biotechnology, The University of Manchester, 131 Princess Street, Manchester, M1 7DN, UK. helen.toogood@manchester.ac.uk.
C3 Biotechnologies Ltd, 20 Mannin Way, Caton Road, Lancaster, LA1 35W, Lancashire, UK. helen.toogood@manchester.ac.uk.

Nigel S Scrutton (NS)

Manchester Institute of Biotechnology, The University of Manchester, 131 Princess Street, Manchester, M1 7DN, UK. nigel.scrutton@manchester.ac.uk.
C3 Biotechnologies Ltd, 20 Mannin Way, Caton Road, Lancaster, LA1 35W, Lancashire, UK. nigel.scrutton@manchester.ac.uk.

Classifications MeSH