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Volume 8, Issue 9

identification of bacterial seaweed-degrading bioplastic producers Open Access

Due to an error in the order of citations the Version of Record of this article has been corrected. The erratum detailing the extent of the corrections can be found here: https://doi.org/10.1099/mgen.0.001195

Abstract

There is an urgent need to replace petroleum-based plastic with bio-based and biodegradable alternatives. Polyhydroxyalkanoates (PHAs) are attractive prospective replacements that exhibit desirable mechanical properties and are recyclable and biodegradable in terrestrial and marine environments. However, the production costs today still limit the economic sustainability of the PHA industry. Seaweed cultivation represents an opportunity for carbon capture, while also supplying a sustainable photosynthetic feedstock for PHA production. We mined existing gene and protein databases to identify bacteria able to grow and produce PHAs using seaweed-derived carbohydrates as substrates. There were no significant relationships between the genes involved in the deconstruction of algae polysaccharides and PHA production, with poor to negative correlations and diffused clustering suggesting evolutionary compartmentalism. We identified 2 987 bacterial candidates spanning 40 taxonomic families predominantly within Alphaproteobacteria, Gammaproteobacteria and Burkholderiales with enriched seaweed-degrading capacity that also harbour PHA synthesis potential. These included highly promising candidates with specialist and generalist specificities, including , , , , , , , , , , , , , , , , , , , , and . In this enriched subset, the family-level densities of genes targeting green macroalgae polysaccharides were considerably higher (=231.6±68.5) than enzymes targeting brown (=65.34±13.12) and red (=30.5±10.72) polysaccharides. Within these organisms, an abundance of genes was observed, suggesting that the fatty acid synthesis pathway supplies (R)−3-hydroxyacyl-CoA or 3-hydroxybutyryl-CoA from core metabolic processes and is the predominant mechanism of PHA production in these organisms. Our results facilitate extending seaweed biomass valorization in the context of consolidated biorefining for the production of bioplastics.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): algae , bioplastic , genome , macroalgae , marine , PHA , polyhydroxyalkanoates and seaweed
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.

Erratum

An erratum has been published for this content:
Erratum: identification of bacterial seaweed-degrading bioplastic producers
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References

  1. Lebreton L, Andrady A. Future scenarios of global plastic waste generation and disposal. Palgrave Commun 2019; 5:11 [View Article]
     [Google Scholar]
  2. Barron A, Sparks TD. Commercial marine-degradable polymers for flexible packaging. iScience 2020; 23:101353 [View Article]
     [Google Scholar]
  3. Bucci K, Tulio M, Rochman CM. What is known and unknown about the effects of plastic pollution: a meta-analysis and systematic review. Ecol Appl 2020; 30:e02044 [View Article]
     [Google Scholar]
  4. Galloway TS, Cole M, Lewis C. Interactions of microplastic debris throughout the marine ecosystem. Nat Ecol Evol 2017; 1:116 [View Article]
     [Google Scholar]
  5. Thushari GGN, Senevirathna JDM. Plastic pollution in the marine environment. Heliyon 2020; 6:e04709 [View Article] [PubMed]
     [Google Scholar]
  6. Choi SY, Rhie MN, Kim HT, Joo JC, Cho IJ et al. Metabolic engineering for the synthesis of polyesters: 100-year journey from polyhydroxyalkanoates to non-natural microbial polyesters. Metab Eng 2020; 58:47–81 [View Article]
     [Google Scholar]
  7. Alcântara JMG, Distante F, Storti G, Moscatelli D, Morbidelli M et al. Current trends in the production of biodegradable bioplastics: the case of polyhydroxyalkanoates. Biotechnol Adv 2020; 42:107582 [View Article]
     [Google Scholar]
  8. Chavan S, Yadav B, Tyagi RD, Drogui P. A review on production of polyhydroxyalkanoate (PHA) biopolyesters by thermophilic microbes using waste feedstocks. Bioresour Technol 2021; 341:125900 [View Article]
     [Google Scholar]
  9. Sirohi R, Lee JS, Yu BS, Roh H, Sim SJ. Sustainable production of polyhydroxybutyrate from autotrophs using CO2 as feedstock: hallenges and opportunities. Bioresour Technol 2021; 341:125751 [View Article]
     [Google Scholar]
  10. Yan X, Li DN, Ma XJ, Li JN. Bioconversion of renewable lignocellulosic biomass into multicomponent substrate via pressurized hot water pretreatment for bioplastic polyhydroxyalkanoate accumulation. Bioresour Technol 2021; 339:125667 [View Article]
     [Google Scholar]
  11. Tan D, Wang Y, Tong Y, Chen GQ. Grand challenges for industrializing polyhydroxyalkanoates (PHAs). Trends Biotechnol 2021; 39:953–963 [View Article]
     [Google Scholar]
  12. Laurens LML, Lane M, Nelson RS. Sustainable seaweed biotechnology solutions for carbon capture, composition, and deconstruction. Trends Biotechnol 2020; 38:1232–1244 [View Article]
     [Google Scholar]
  13. Fidai YA, Dash J, Tompkins EL, Tonon T. A systematic review of floating and beach landing records of Sargassum beyond the Sargasso Sea. Environ Res Commun 2020; 2:122001 [View Article]
     [Google Scholar]
  14. Markets Ra. Outlook on the Commercial Seaweeds Global Market to 2028: Research and Markets; 2021 https://www.businesswire.com/news/home/20211110005992/en/Outlook-on-the-Commercial-Seaweeds-Global-Market-to-2028---by-Type[1]Method-of-Harvesting-Form-Application-and-Region---ResearchAndMarkets.com
  15. Algaia Product optimization: Algaia; 2021 https://www.algaia.com/index.php/by-products-optimization/
  16. Wei N, Quarterman J, Jin Y-S. Marine macroalgae: an untapped resource for producing fuels and chemicals. Trends Biotechnol 2013; 31:70–77 [View Article]
     [Google Scholar]
  17. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 2014; 42:D490–5 [View Article] [PubMed]
     [Google Scholar]
  18. Becker S, Tebben J, Coffinet S, Wiltshire K, Iversen MH et al. Laminarin is a major molecule in the marine carbon cycle. Proc Natl Acad Sci U S A 2020; 117:6599–6607 [View Article] [PubMed]
     [Google Scholar]
  19. Dudek M, Dieudonné A, Jouanneau D, Rochat T, Michel G et al. Regulation of alginate catabolism involves a GntR family repressor in the marine flavobacterium Zobellia galactanivorans DsijT. Nucleic Acids Res 2020; 48:7786–7800 [View Article] [PubMed]
     [Google Scholar]
  20. Sichert A, Corzett CH, Schechter MS, Unfried F, Markert S et al. Verrucomicrobia use hundreds of enzymes to digest the algal polysaccharide fucoidan. Nat Microbiol 2020; 5:1026–1039 [View Article]
     [Google Scholar]
  21. Ficko-Blean E, Préchoux A, Thomas F, Rochat T, Larocque R et al. Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria. Nat Commun 2017; 8:1685 [View Article]
     [Google Scholar]
  22. Hettle AG, Hobbs JK, Pluvinage B, Vickers C, Abe KT et al. Insights into the κ/ι-carrageenan metabolism pathway of some marine Pseudoalteromonas species. Commun Biol 2019; 2:474 [View Article] [PubMed]
     [Google Scholar]
  23. Christiansen L, Pathiraja D, Bech PK, Schultz-Johansen M, Hennessy R et al. A multifunctional polysaccharide utilization gene cluster in Colwellia echini encodes enzymes for the complete degradation of κ-Carrageenan, ι-Carrageenan, and Hybrid β/κ-Carrageenan. mSphere 2020; 5:e00792-19 [View Article]
     [Google Scholar]
  24. Reisky L, Préchoux A, Zühlke M-K, Bäumgen M, Robb CS et al. A marine bacterial enzymatic cascade degrades the algal polysaccharide ulvan. Nat Chem Biol 2019; 15:803–812 [View Article]
     [Google Scholar]
  25. El-Malek FA, Khairy H, Farag A, Omar S. The sustainability of microbial bioplastics, production and applications. Int J Biol Macromol 2020; 157:319–328 [View Article] [PubMed]
     [Google Scholar]
  26. Bera A, Dubey S, Bhayani K, Mondal D, Mishra S et al. Microbial synthesis of polyhydroxyalkanoate using seaweed-derived crude levulinic acid as co-nutrient. Int J Biol Macromol 2015; 72:487–494 [View Article] [PubMed]
     [Google Scholar]
  27. Alkotaini B, Koo H, Kim BS. Production of polyhydroxyalkanoates by batch and fed-batch cultivations of Bacillus megaterium from acid-treated red algae. Korean J Chem Eng 2016; 33:1669–1673 [View Article]
     [Google Scholar]
  28. Azizi N, Najafpour G, Younesi H. Acid pretreatment and enzymatic saccharification of brown seaweed for polyhydroxybutyrate (PHB) production using Cupriavidus necator. Int J Biol Macromol 2017; 101:1029–1040 [View Article] [PubMed]
     [Google Scholar]
  29. Sawant SS, Salunke BK, Kim BS. Consolidated bioprocessing for production of polyhydroxyalkanotes from red algae Gelidium amansii. Int J Biol Macromol 2018; 109:1012–1018 [View Article] [PubMed]
     [Google Scholar]
  30. Yamaguchi T, Narsico J, Kobayashi T, Inoue A, Ojima T. Production of poly(3-hydroyxybutylate) by a novel alginolytic bacterium Hydrogenophaga sp. strain UMI-18 using alginate as a sole carbon source. J Biosci Bioeng 2019; 128:203–208 [View Article] [PubMed]
     [Google Scholar]
  31. Moriya H, Takita Y, Matsumoto A, Yamahata Y, Nishimukai M et al. Cobetia sp. bacteria, which are capable of utilizing alginate or waste Laminaria sp. for poly(3-hydroxybutrate) synthesis, isolated from a marine environment. Front Bioeng Biotechnol 2020; 8:974 [View Article] [PubMed]
     [Google Scholar]
  32. Pu N, Hu P, Shi L-L, Li Z-J. Microbial production of poly(3-hydroxybutyrate) from volatile fatty acids using the marine bacterium Neptunomonas concharum. Bioresour Technol Rep 2020; 11:100439 [View Article]
     [Google Scholar]
  33. Tůma S, Izaguirre J, Bondar M, Marques M, Fernandes P et al. Upgrading end-of-line residues of the red seaweed Gelidium sesquipedale to polyhydroxyalkanoates using Halomonas boliviensis. Biotechnol Rep 2020; 27:e00491 [View Article] [PubMed]
     [Google Scholar]
  34. Mostafa YS, Alrumman SA, Alamri SA, Otaif KA, Mostafa MS et al. Bioplastic (poly-3-hydroxybutyrate) production by the marine bacterium Pseudodonghicola xiamenensis through date syrup valorization and structural assessment of the biopolymer. Sci Rep 2020; 10:8815 [View Article] [PubMed]
     [Google Scholar]
  35. Ghosh S, Gnaim R, Greiserman S, Fadeev L, Gozin M et al. Macroalgal biomass subcritical hydrolysates for the production of polyhydroxyalkanoate (PHA) by Haloferax mediterranei. Bioresour Technol 2019; 271:166–173 [View Article] [PubMed]
     [Google Scholar]
  36. Ghosh S, Greiserman S, Chemodanov A, Slegers PM, Belgorodsky B et al. Polyhydroxyalkanoates and biochar from green macroalgal Ulva sp. biomass subcritical hydrolysates: process optimization and a priori economic and greenhouse emissions break-even analysis. Sci Total Environ 2021; 770:145281 [View Article] [PubMed]
     [Google Scholar]
  37. Ghosh S, Coons J, Yeager C, Halley P, Chemodanov A et al. Halophyte biorefinery for polyhydroxyalkanoates production from Ulva sp. hydrolysate with Haloferax mediterranei in pneumatically agitated bioreactors and ultrasound harvesting. Bioresour Technol 2021125964 [View Article] [PubMed]
     [Google Scholar]
  38. Steinbruch E, Drabik D, Epstein M, Ghosh S, Prabhu MS et al. Hydrothermal processing of a green seaweed Ulva sp. for the production of monosaccharides, polyhydroxyalkanoates, and hydrochar. Bioresour Technol 2020; 318:124263 [View Article] [PubMed]
     [Google Scholar]
  39. Gnaim R, Polikovsky M, Unis R, Sheviryov J, Gozin M et al. Marine bacteria associated with the green seaweed Ulva sp. for the production of polyhydroxyalkanoates. Bioresour Technol 2021; 328:124815 [View Article] [PubMed]
     [Google Scholar]
  40. Jeong DW, Hyeon JE, Lee M-E, Ko YJ, Kim M et al. Efficient utilization of brown algae for the production of polyhydroxybutyrate (PHB) by using an enzyme complex immobilized on Ralstonia eutropha. Int J Biol Macromol 2021; 189:819–825 [View Article] [PubMed]
     [Google Scholar]
  41. Muhammad M, Aloui H, Khomlaem C, Hou CT, Kim BS. Production of polyhydroxyalkanoates and carotenoids through cultivation of different bacterial strains using brown algae hydrolysate as a carbon source. Biocatal Agric Biotechnol 2020; 30:101852 [View Article]
     [Google Scholar]
  42. Zhang H, Yohe T, Huang L, Entwistle S, Wu P et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 2018; 46:W95–W101 [View Article] [PubMed]
     [Google Scholar]
  43. Huerta-Cepas J, Serra F, Bork P. ETE 3: reconstruction, analysis, and visualization of phylogenomic data. Mol Biol Evol 2016; 33:1635–1638 [View Article] [PubMed]
     [Google Scholar]
  44. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
     [Google Scholar]
  45. O’Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res 2016; 44:D733–45 [View Article] [PubMed]
     [Google Scholar]
  46. Hagberg A, Swart P, S Chult D. Exploring Network Structure, Dynamics, and Function Using NetworkX Los Alamos, NM (United States): Los Alamos National Lab.(LANL); 2008
     [Google Scholar]
  47. Peixoto TP. The graph-tool python library. Figshare 2014
     [Google Scholar]
  48. Sun ZZ, Ji BW, Zheng N, Wang M, Cao Y et al. Phylogenetic distribution of polysaccharide-degrading enzymes in marine bacteria. Front Microbiol 2021; 12:658620 [View Article] [PubMed]
     [Google Scholar]
  49. Wu M, Scott AJ. Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. Bioinformatics 2012; 28:1033–1034 [View Article] [PubMed]
     [Google Scholar]
  50. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
     [Google Scholar]
  51. Pedregosa F, Varoquaux G, Gramfort A, Michel V, Thirion B et al. Scikit-learn: machine learning in python; 2011; 122825–2830
  52. Buitinck L, Louppe G, Blondel M, Pedregosa F, Mueller A et al. API design for machine learning software: experiences from the Scikit-learn project. arXiv preprint arXiv 201313090238
     [Google Scholar]
  53. Shaw DK, Sekar J, Ramalingam PV. Recent insights into oceanic dimethylsulfoniopropionate biosynthesis and catabolism. Environ Microbiol 2022; 24:2669–2700 [View Article] [PubMed]
     [Google Scholar]
  54. Roja K, Ruben Sudhakar D, Anto S, Mathimani T. Extraction and characterization of polyhydroxyalkanoates from marine green alga and cyanobacteria. Biocatal Agric Biotechnol 2019; 22:101358 [View Article]
     [Google Scholar]
  55. Abd El-malek F, Rofeal M, Farag A, Omar S, Khairy H. Polyhydroxyalkanoate nanoparticles produced by marine bacteria cultivated on cost effective Mediterranean algal hydrolysate media. J Biotechnol 2021; 328:95–105 [View Article] [PubMed]
     [Google Scholar]
  56. Wang YY, Zhao FJ, Fan X, Wang SF, Song CJ. Enhancement of medium-chain-length polyhydroxyalkanoates biosynthesis from glucose by metabolic engineering in Pseudomonas mendocina. Biotechnol Lett 2016; 38:313–320 [View Article] [PubMed]
     [Google Scholar]
  57. Li HL, Deng RX, Wang W, Liu KQ, Hu HB et al. Biosynthesis and characterization of medium-chain-length polyhydroxyalkanoate with an enriched 3-hydroxydodecanoate monomer from a Pseudomonas chlororaphis cell factory. J Agric Food Chem 2021; 69:3895–3903 [View Article] [PubMed]
     [Google Scholar]
  58. Zhang Y, Liu H, Liu Y, Huo K, Wang S et al. A promoter engineering-based strategy enhances polyhydroxyalkanoate production in Pseudomonas putida KT2440. Int J Biol Macromol 2021; 191:608–617 [View Article] [PubMed]
     [Google Scholar]
  59. Zhao F, Liu X, Kong A, Zhao Y, Fan X et al. Screening of endogenous strong promoters for enhanced production of medium-chain-length polyhydroxyalkanoates in Pseudomonas mendocina NK-01. Sci Rep 2019; 9:1798 [View Article] [PubMed]
     [Google Scholar]
  60. Villano M, Beccari M, Dionisi D, Lampis S, Miccheli A et al. Effect of pH on the production of bacterial polyhydroxyalkanoates by mixed cultures enriched under periodic feeding. Process Biochem 2010; 45:714–723 [View Article]
     [Google Scholar]
  61. Wang YP, Cai JY, Lan JH, Liu ZG, He N et al. Biosynthesis of poly(hydroxybutyrate-hydroxyvalerate) from the acclimated activated sludge and microbial characterization in this process. Bioresour Technol 2013; 148:61–69 [View Article] [PubMed]
     [Google Scholar]
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In silico identification of bacterial seaweed-degrading bioplastic producers
M Gen 8, 000866 (2022); https://doi.org/10.1099/mgen.0.000866
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