Widespread distribution of bacteria containing PETases with a functional motif across global oceans.

Journal: The ISME journal
Published Date:

Abstract

Accumulating evidence indicates that microorganisms respond to the ubiquitous plastic pollution by evolving plastic-degrading enzymes. However, the functional diversity of these enzymes and their distribution across the ocean, including the deep sea, remain poorly understood. By integrating bioinformatics and artificial intelligence-based structure prediction, we developed a structure- and function-informed algorithm to computationally distinguish functional polyethylene terephthalate-degrading enzymes (PETases) from variants lacking PETase activity (pseudo-PETase), either due to alternative substrate specificity or pseudogene origin. Through in vitro functional screening and in vivo microcosm experiments, we verified that this algorithm identified a high-confidence, searchable sequence motif for functional PETases capable of degrading PET. Metagenomic analysis of 415 ocean samples revealed 23 PETase variants, detected in nearly 80% of the samples. These PETases mainly occur between 1000 and 2000 m deep and at the surface in regions with high plastic pollution. Metatranscriptomic analysis further identified PETase variants that were actively transcribed by marine microorganisms. In contrast to their terrestrial counterparts-where PETases are taxonomically diverse-those in marine ecosystems were predominantly encoded and transcribed by members of the Pseudomonadales order. Our study underscores the widespread distribution of PETase-containing bacteria across carbon-limited marine ecosystems, identifying and distinguishing the PETase motif that underpins the functionality of these specialised cutinases.

Authors

  • Intikhab Alam
    Center of Excellence for Smart Health, Computer, Electrical and Mathematical Science and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
  • Ramona Marasco
    Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
  • Afaque A Momin
    Center of Excellence for Smart Health, Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
  • Nojood Aalismail
    Marine Science Program, Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
  • Elisa Laiolo
    Marine Science Program, Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
  • Cecilia Martin
    Marine Science Program, Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
  • Isabel Sanz-Sáez
    Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar-CSIC, Pg. Marítim de la Barceloneta 37-49, 08003, Barcelona, Spain.
  • Begoña Baltá Foix
    Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar-CSIC, Pg. Marítim de la Barceloneta 37-49, 08003, Barcelona, Spain.
  • Elisabet L Sá
    Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar-CSIC, Pg. Marítim de la Barceloneta 37-49, 08003, Barcelona, Spain.
  • Allan Kamau
    Center of Excellence for Smart Health, Computer, Electrical and Mathematical Science and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
  • Francisco J Guzmán-Vega
    Bioscience Program, Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Kingdom of Saudi Arabia.
  • Tahira Jamil
    Center of Excellence for Smart Health, Computer, Electrical and Mathematical Science and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
  • Silvia G Acinas
    Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar-CSIC, Pg. Marítim de la Barceloneta 37-49, 08003, Barcelona, Spain.
  • Josep M Gasol
    Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar-CSIC, Pg. Marítim de la Barceloneta 37-49, 08003, Barcelona, Spain.
  • Takashi Gojobori
    Center of Excellence on Smart Health, King Abdullah University of Science and Technology (KAUST), 23955-6900 Thuwal, Kingdom of Saudi Arabia.
  • Susana Agusti
    Marine Science Program, Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
  • Daniele Daffonchio
    Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
  • Stefan T Arold
    Bioscience Program, Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Kingdom of Saudi Arabia.
  • Carlos M Duarte
    Computational Bioscience Research Center (CBRC), Computer, Electrical and Mathematical Sciences and Engineering (CEMSE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, 23955, Saudi Arabia.

Keywords

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