IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33566-5.html
   My bibliography  Save this article

A pathway for chitin oxidation in marine bacteria

Author

Listed:
  • Wen-Xin Jiang

    (Shandong University
    Ocean University of China)

  • Ping-Yi Li

    (Shandong University
    Pilot National Laboratory for Marine Science and Technology)

  • Xiu-Lan Chen

    (Shandong University
    Pilot National Laboratory for Marine Science and Technology)

  • Yi-Shuo Zhang

    (Shandong University)

  • Jing-Ping Wang

    (Shandong University)

  • Yan-Jun Wang

    (Shandong University)

  • Qi Sheng

    (Shandong University)

  • Zhong-Zhi Sun

    (Shandong University)

  • Qi-Long Qin

    (Shandong University
    Pilot National Laboratory for Marine Science and Technology)

  • Xue-Bing Ren

    (Shandong University)

  • Peng Wang

    (Ocean University of China
    Pilot National Laboratory for Marine Science and Technology)

  • Xiao-Yan Song

    (Shandong University)

  • Yin Chen

    (Ocean University of China
    University of Warwick)

  • Yu-Zhong Zhang

    (Ocean University of China
    Pilot National Laboratory for Marine Science and Technology
    Shandong University)

Abstract

Oxidative degradation of chitin, initiated by lytic polysaccharide monooxygenases (LPMOs), contributes to microbial bioconversion of crystalline chitin, the second most abundant biopolymer in nature. However, our knowledge of oxidative chitin utilization pathways, beyond LPMOs, is very limited. Here, we describe a complete pathway for oxidative chitin degradation and its regulation in a marine bacterium, Pseudoalteromonas prydzensis. The pathway starts with LPMO-mediated extracellular breakdown of chitin into C1-oxidized chitooligosaccharides, which carry a terminal 2-(acetylamino)−2-deoxy-D-gluconic acid (GlcNAc1A). Transmembrane transport of oxidized chitooligosaccharides is followed by their hydrolysis in the periplasm, releasing GlcNAc1A, which is catabolized in the cytoplasm. This pathway differs from the known hydrolytic chitin utilization pathway in enzymes, transporters and regulators. In particular, GlcNAc1A is converted to 2-keto-3-deoxygluconate 6-phosphate, acetate and NH3 via a series of reactions resembling the degradation of D-amino acids rather than other monosaccharides. Furthermore, genomic and metagenomic analyses suggest that the chitin oxidative utilization pathway may be prevalent in marine Gammaproteobacteria.

Suggested Citation

  • Wen-Xin Jiang & Ping-Yi Li & Xiu-Lan Chen & Yi-Shuo Zhang & Jing-Ping Wang & Yan-Jun Wang & Qi Sheng & Zhong-Zhi Sun & Qi-Long Qin & Xue-Bing Ren & Peng Wang & Xiao-Yan Song & Yin Chen & Yu-Zhong Zhan, 2022. "A pathway for chitin oxidation in marine bacteria," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33566-5
    DOI: 10.1038/s41467-022-33566-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33566-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-33566-5?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Tien-Chye Tan & Daniel Kracher & Rosaria Gandini & Christoph Sygmund & Roman Kittl & Dietmar Haltrich & B. Martin Hällberg & Roland Ludwig & Christina Divne, 2015. "Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    2. Federico Sabbadin & Glyn R. Hemsworth & Luisa Ciano & Bernard Henrissat & Paul Dupree & Theodora Tryfona & Rita D. S. Marques & Sean T. Sweeney & Katrin Besser & Luisa Elias & Giovanna Pesante & Yi Li, 2018. "An ancient family of lytic polysaccharide monooxygenases with roles in arthropod development and biomass digestion," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    3. Manuel Eibinger & Jürgen Sattelkow & Thomas Ganner & Harald Plank & Bernd Nidetzky, 2017. "Single-molecule study of oxidative enzymatic deconstruction of cellulose," Nature Communications, Nature, vol. 8(1), pages 1-7, December.
    4. Tim N. Enke & Gabriel E. Leventhal & Matthew Metzger & José T. Saavedra & Otto X. Cordero, 2018. "Microscale ecology regulates particulate organic matter turnover in model marine microbial communities," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    5. C. Manno & S. Fielding & G. Stowasser & E. J. Murphy & S. E. Thorpe & G. A. Tarling, 2020. "Continuous moulting by Antarctic krill drives major pulses of carbon export in the north Scotia Sea, Southern Ocean," Nature Communications, Nature, vol. 11(1), pages 1-8, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Zihao Zhao & Chie Amano & Thomas Reinthaler & Federico Baltar & Mónica V. Orellana & Gerhard J. Herndl, 2024. "Metaproteomic analysis decodes trophic interactions of microorganisms in the dark ocean," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Ho Ta Giap & Ngo Nguyen Vu & Vu Van Van, 2023. "Isolation and identification of Vibrio spp. with potential ability to produce polysaccharide monooxygenase from diseased Penaeus monodon," HO CHI MINH CITY OPEN UNIVERSITY JOURNAL OF SCIENCE - ENGINEERING AND TECHNOLOGY, HO CHI MINH CITY OPEN UNIVERSITY JOURNAL OF SCIENCE, HO CHI MINH CITY OPEN UNIVERSITY, vol. 13(1), pages 24-32.
    2. Chujin Ruan & Josep Ramoneda & Anton Kan & Timothy J. Rudge & Gang Wang & David R. Johnson, 2024. "Phage predation accelerates the spread of plasmid-encoded antibiotic resistance," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Zihao Zhao & Chie Amano & Thomas Reinthaler & Federico Baltar & Mónica V. Orellana & Gerhard J. Herndl, 2024. "Metaproteomic analysis decodes trophic interactions of microorganisms in the dark ocean," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Iván Ayuso-Fernández & Tom Z. Emrich-Mills & Julia Haak & Ole Golten & Kelsi R. Hall & Lorenz Schwaiger & Trond S. Moe & Anton A. Stepnov & Roland Ludwig & George E. Cutsail III & Morten Sørlie & Åsmu, 2024. "Mutational dissection of a hole hopping route in a lytic polysaccharide monooxygenase (LPMO)," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    5. Nora-Charlotte Pauli & Clara M. Flintrop & Christian Konrad & Evgeny A. Pakhomov & Steffen Swoboda & Florian Koch & Xin-Liang Wang & Ji-Chang Zhang & Andrew S. Brierley & Matteo Bernasconi & Bettina M, 2021. "Krill and salp faecal pellets contribute equally to the carbon flux at the Antarctic Peninsula," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    6. Moira Décima & Michael R. Stukel & Scott D. Nodder & Andrés Gutiérrez-Rodríguez & Karen E. Selph & Adriana Lopes dos Santos & Karl Safi & Thomas B. Kelly & Fenella Deans & Sergio E. Morales & Federico, 2023. "Salp blooms drive strong increases in passive carbon export in the Southern Ocean," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Mohammad Bahadori & Chengrong Chen & Stephen Lewis & Juntao Wang & Jupei Shen & Enqing Hou & Mehran Rezaei Rashti & Qiaoyun Huang & Zoe Bainbridge & Tom Stevens, 2023. "The origin of suspended particulate matter in the Great Barrier Reef," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    8. Trang T. H. Nguyen & Emily J. Zakem & Ali Ebrahimi & Julia Schwartzman & Tolga Caglar & Kapil Amarnath & Uria Alcolombri & François J. Peaudecerf & Terence Hwa & Roman Stocker & Otto X. Cordero & Naom, 2022. "Microbes contribute to setting the ocean carbon flux by altering the fate of sinking particulates," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    9. Yichao Wu & Chengxia Fu & Caroline L. Peacock & Søren J. Sørensen & Marc A. Redmile-Gordon & Ke-Qing Xiao & Chunhui Gao & Jun Liu & Qiaoyun Huang & Zixue Li & Peiyi Song & Yongguan Zhu & Jizhong Zhou , 2023. "Cooperative microbial interactions drive spatial segregation in porous environments," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    10. Matthew S. Savoca & Mehr Kumar & Zephyr Sylvester & Max F. Czapanskiy & Bettina Meyer & Jeremy A. Goldbogen & Cassandra M. Brooks, 2024. "Whale recovery and the emerging human-wildlife conflict over Antarctic krill," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    11. Fondi, Marco & Di Patti, Francesca, 2019. "A synthetic ecosystem for the multi-level modelling of heterotroph-phototroph metabolic interactions," Ecological Modelling, Elsevier, vol. 399(C), pages 13-22.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33566-5. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.