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Research Article | Open Access

Safety evaluation and whole genome sequencing for revealing the ability of Penicillium oxalicum WX-209 to safely and effectively degrade citrus segments

Xiao Hua,1, Yujiao Qiana,1, Zhipeng Gaob, Gaoyang Lia, Fuhua Fua, Jiajing Guoa( ), Yang Shana( )
Hunan Agriculture Product Processing Institute, International Joint Lab on Fruits & Vegetables Processing, Quality and Safety, Hunan Key Lab of Fruits & Vegetables Storage, Processing, Quality and Safety, Hunan Academy of Agricultural Sciences, Changsha 410125, China
College of Animal Science and Technology, Hunan Agricultural University, Changsha 410128, China

1 These authors contributed equally to this work.

Peer review under responsibility of KeAi Communications Co., Ltd.

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Abstract

The microbial potential of Penicillium has received critical attention. The present research aimed to elucidate the efficacy of crude enzyme secreted from Penicillium oxalicum WX-209 in degrading citrus segments and evaluate the safety of the process. Results showed that citrus segment membranes gradually dissolved after treatment with the crude enzyme solution, indicating good degradation capability. No significant differences in body weight, food ingestion rate, hematology, blood biochemistry, and weight changes of different organs were found between the enzyme intake and control groups. Serial experiments showed that the crude enzyme had high biological safety. Moreover, the whole genome of P. oxalicum WX-209 was sequenced by PacBio and Illumina platforms. Twenty-five scaffolds were assembled to generate 36 Mbp size of genome sequence comprising 11369 predicted genes modeled with a GC content of 48.33%. A total of 592 genes were annotated to encode enzymes related to carbohydrates, and some degradation enzyme genes were identified in strain P. oxalicum WX-209.

Keywords

DegradationSafety evaluation Penicillium oxalicum WX-209Crude enzymeGenome sequencing

References

[1]

L. Coll-Almela, D. Saura-Lopez, J. Laencina-Sanchez, et al., Characterisation of cell-wall polysaccharides from mandarin segment membranes. Food Chem. 175 (2015) 36-42. https://doi.org/10.1016/j.foodchem.2014.11.118.
Crossref Google Scholar
[2]

F. Liu, A. Osman, S. Yusof, et al., Effects of enzyme-aided peeling on the quality of local mandarin (Citrus Reticulata B.) segments. J. Food Process. Pres. 28 (2004) 336-347. https://doi.org/10.1111/j.1745-4549.2004.21145.x.
Crossref Google Scholar
[3]

D. Martinez, R.M. Berka, B. Henrissat, et al., Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat. Biotechnol. 26(5) (2008) 553-560. https://doi.org/10.1038/nbt1008-1193a.
Crossref Google Scholar
[4]

R.K. Prasad, S. Chatterjee, P.B. Mazumder, et al., Bioethanol production from waste lignocelluloses: a review on microbial degradation potential. Chemosphere 231 (2019) 588-606. https://doi.org/10.1016/j.chemosphere.2019.05.142.
Crossref Google Scholar
[5]

B.B. Chi, Y.N. Lu, P.C. Yin, et al., Sequencing and Comparative genomic analysis of a highly metal-tolerant Penicillium janthinellum P1 provide insights into its metal tolerance. Front. Microbiol. 12 (2021) 663217. https://doi.org/10.3389/fmicb.2021.663217.
Crossref Google Scholar
[6]

R.H. Bischof, J. Ramoni, B. Seiboth, Cellulases and beyond: the first 70 years of the enzyme producer Trichoderma reesei. Microb. Cell Fact. 15(1) (2016) 106. https://doi.org/10.1186/s12934-016-0507-6.
Crossref Google Scholar
[7]

E.S. Martens-Uzunova, P.J. Schaap, Assessment of the pectin degrading enzyme network of Aspergillus niger by functional genomics. Fungal Genet. Biol. 46 (2009) S170-S179. https://doi.org/10.1016/j.fgb.2008.07.021.
Crossref Google Scholar
[8]

J.Y. Wang, Z.P. Gao, Y.J. Qian, et al., Citrus segment degradation potential, enzyme safety evaluation, and whole genome sequence of Aspergillus aculeatus strain ZC-1005. Frontiers in Microbiology 12 (2021) 671200. https://doi.org/10.3389/fmicb.2021.671200.
Crossref Google Scholar
[9]

Y.J. Qian, Z.P. Gao, J.Y. Wang, et al., Safety evaluation and whole genome sequencing of Aspergillus japonicas PJ01 reveal its potential to degrade citrus segments in juice processing. Foods 10(8) (2021) 1736. https://doi.org/10.3390/foods10081736.
Crossref Google Scholar
[10]

G. Liu, Y. Qin, Z. Li, et al., Improving lignocellulolytic enzyme production with Penicillium: from strain screening to systems biology. Biofuels. 4(5) (2013) 523-534. https://doi.org/10.4155/bfs.13.38.
Crossref Google Scholar
[11]

S. Grijseels, J. Nielsen, J.C. Nielsen, et al., Penicillium arizonense, a new, genome sequenced fungal species, reveals a high chemical diversity in secreted metabolites. Sci. Rep. 6 (2016) 35112. https://doi.org/10.1038/srep35112.
Crossref Google Scholar
[12]

W.D.H. Schneider, T.A. Gonçalves, C.A. Uchima, et al., Penicillium echinulatum secretome analysis reveals the fungi potential for degradation of lignocellulosic biomass. Biotechnol Biofuels. 9 (2016) 66. https://doi.org/10.1186/s13068-016-0476-3.
Crossref Google Scholar
[13]

D.R. Olicón-Hernández, C. Gómez-Silván, C. Pozo, et al., Penicillium oxalicum XD-3.1 removes pharmaceutical compounds from hospital wastewater and outcompetes native bacterial and fungal communities in fluidised batch bioreactors. International Biodeterioration & Biodegradation 158 (2021) 105179. https://doi.org/10.1016/j.ibiod.2021.105179.
Crossref Google Scholar
[14]

L. Santi, W.O. Beys-Da-Silva, M. Berger, et al., Penicillium oxalicum secretomic analysis identify plant cell wall degrading enzymes important for fruit juice extraction. Journal of Food Science and Technology 58(5) (2020) 1764-1775. https://doi.org/10.1007/s13197-020-04688-9.
Crossref Google Scholar
[15]

W.J. Jiang, W. Liu, Y.H. Li, et al., Citrinin impairs pig oocyte maturation by inducing oxidative stress and apoptosis. Toxicon 205 (2022) 84-90. https://doi.org/10.1016/j.toxicon.2021.11.124
Crossref Google Scholar
[16]

S.J. Luo, H.L. Du, H. Kebede, et al., Contamination status of major mycotoxins in agricultural product and food stuff in Europe. Food Control 127 (2021) 108120. https://doi.org/10.1016/j.foodcont.2021.108120
Crossref Google Scholar
[17]

N. Hussain, I. Ishak, M.A.A. Kamal, et al., Peeling of key lime (Citrus aurantifolia) fruit aided with vacuum infusion, different levels of pectinase concentration and soaking time. Journal of Food Measurement and Characterization 13(3) (2019) 2095-2105. https://doi.org/10.1007/s11694-019-00130-7.
Crossref Google Scholar
[18]
P. Li, G. Li, C. Zhang, et al. New Penicillium oxalicum strain WX-209 useful for producing high-yield cellulase[P]. CN103468583-A, 2013-08-13.
[19]

C.X. Li, S. Zhao, T. Zhang, et al., Genome sequencing and analysis of Talaromyces pinophilus provide insights into biotechnological applications. Sci. Rep. 7(1) (2017) 490. https://doi.org/10.1038/s41598-017-00567-0.
Crossref Google Scholar
[20]

S. Zhao, Y.S. Yan, Q.P. He, et al., Comparative genomic, transcriptomic and secretomic profiling of Penicillium oxalicum HP7-1 and its cellulase and xylanase hyper-producing mutant EU2106, and identification of two novel regulatory genes of cellulase and xylanase gene expression. Biotechnol Biofuels. 9 (2016) 203. https://doi.org/10.1186/s13068-016-0616-9.
Crossref Google Scholar
[21]

X. Wang, L. Lin, Y. Tang, et al., Transcriptomic insights into citrus segment membrane's cell wall components relating to fruit sensory texture. BMC Genomics. 19(1) (2018) 280. https://doi.org/10.1186/s12864-018-4669-y.
Crossref Google Scholar
[22]

V. Silano, J.M. Barat Baviera, C. Bolognesi, et al., Safety evaluation of the food enzyme xylanase from the genetically modified Aspergillus luchuensis Inui strain RF7398. EFSA Journal 18(1) (2020) e05971. https://doi.org/10.2903/j.efsa.2020.5971.
Crossref Google Scholar
[23]

A. Kern, D. Shanahan, R. Buesen, et al., Safety evaluation of a β-mannanase enzyme preparation produced with Thermothelomyces thermophilus expressing a protein-engineered β-mannanase gene. PLoS ONE 15(12) (2020) e0243647. https://doi.org/10.1371/journal.pone.0243647.
Crossref Google Scholar
[24]

V. Silano, J.M. Barat Baviera, C. Bolognesi, et al., Safety evaluation of the food enzyme cellulase from the non-genetically modified Penicillium funiculosum strain DP-Lzc35. EFSA Journal 19(1) (2021) e06365. https://doi.org/10.2903/j.efsa.2021.6365.
Crossref Google Scholar
[25]

A. Gryshyna, L. Kautto, R. Peterson, et al., On the safety of filamentous fungi with special emphasis on Trichoderma reesei and products made by recombinant means. Gene Expression Systems in Fungi: Advancements and Applications (2016) 441-457. https://doi.org/10.1007/978-3-319-27951-0_20.
Crossref Google Scholar
[26]

V. Silano, J.M. Barat Baviera, C. Bolognesi, et al., Scientific opinion of the safety evaluation of the food enzyme endo-1,4-β-xylanase from the genetically modified Trichoderma reesei strain RF5427. EFSA Journal 18(6) (2020) 6127. https://doi.org/10.2903/j.efsa.2020.6127.
Crossref Google Scholar
[27]

E. Schuster, N. Dunn-Coleman, J.C. Frisvad, et al., On the safety of Aspergillus niger: a review. Appl. Microbiol. Biotechnol. 59(4/5) (2002) 426-435. https://doi.org/10.1007/bf00183230.
Crossref Google Scholar
[28]

V. Silano, C. Bolognesi, L. Castle, et al., Scientific opinion on the safety evaluation of the food enzyme endo-1,4-β-xylanase from a genetically modified Aspergillus niger (strain XEA). EFSA Journal 16(4) (2018) 5228. https://doi.org/10.2903/j.efsa.2018.5228.
Crossref Google Scholar
[29]

L. Peng, L. Li, X. Liu, et al., Chromosome-level comprehensive genome of mangrove sediment-derived fungus Penicillium variabile HXQ-H-1. J Fungi. 6(1) (2019) 7. https://doi.org/10.3390/jof6010007.
Crossref Google Scholar
[30]

Y. Li, X. Zheng, X. Zhang, et al., The different roles of Penicillium oxalicum LaeA in the production of extracellular cellulase and β-xylosidase. Front Microbiol. 7 (2016) 2091. https://doi.org/10.3389/fmicb.2016.02091.
Crossref Google Scholar
[31]

C.X. Li, S. Zhao, X.M. Luo, et al., Weighted gene co-expression network analysis identifies critical genes for the production of cellulase and xylanase in Penicillium oxalicum. Front Microbiol. 11 (2020) 520. https://doi.org/10.3389/fmicb.2020.00520.
Crossref Google Scholar
[32]

Z. Li, G. Yao, R. Wu, et al., Synergistic and dose-controlled regulation of cellulase gene expression in Penicillium oxalicum. PLoS Genet 11(9) (2015) e1005509. https://doi.org/10.1371/journal.pgen.1005509.
Crossref Google Scholar
[33]

Y. Qin, L. Bao, M. Gao, et al., Penicillium decumbens BrlA extensively regulates secondary metabolism and functionally associates with the expression of cellulase genes. Appl. Microbiol. Biotechnol. 97(24) (2013) 10453-10467. https://doi.org/10.1007/s00253-013-5273-3.
Crossref Google Scholar
[34]

M. Kanehisa, S. Goto, KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28 (2000) 27-30. https://doi.org/10.1093/nar/28.1.27.
Crossref Google Scholar
[35]

S.H. Li, L.S. Gu, X.Y. Qu, et al., Involvement of phospholipase PLA2 in production of cellulase and xylanase by Penicillium oxalicum. Applied Microbiology and Biotechnology 105 (2021) 679-694. https://doi.org/10.1007/s00253-020-11065-1.
Crossref Google Scholar
[36]

S. Zhao, X.Z. Liao, J.X. Wang. Transcription factor Atf1 regulates expression of cellulase and xylanase genes during solid-state fermentation of ascomycetes. Applied and Environmental Microbiology 85(24) (2019) e01226-19. https://doi.org/10.1128/AEM.01226-19.
Crossref Google Scholar
[37]

F. Bhiri, A. Gargouri, M.B. Ali, et al., Molecular cloning, gene expression analysis and structural modelling of the cellobiohydrolase I from Penicillium occitanis. Enzyme and Microbial Technology 46(2) (2010) 74-81. https://doi.org/10.1016/j.enzmictec.2009.10.002.
Crossref Google Scholar
[38]

A.V. Gusakov, Alternatives to Trichoderma reesei in biofuel production. Trends Biotechnol 29(9) (2011) 419-425. https://doi.org/10.1016/j.tibtech.2011.04.004.
Crossref Google Scholar
[39]

C.M. Payne, B.C. Knott, H.B. Mayes, et al., Fungal cellulases. Chem Rev. 115(3) (2015) 1308-1448. https://doi.org/10.1021/cr500351c.
Crossref Google Scholar
[40]

A.V. Bernardi, P.F. de Gouvêa, L.E. Gerolamo, et al., Functional characterization of GH7 endo-1,4-β-glucanase from Aspergillus fumigatus and its potential industrial application. Protein Expr. Purif. 150 (2018) 1-11. https://doi.org/10.1016/j.pep.2018.04.016.
Crossref Google Scholar
[41]

Y. Ye, X. Li, J. Zhao, Production and characteristics of a novel xylose- and alkali-tolerant GH 43 β-xylosidase from Penicillium oxalicum for promoting hemicellulose degradation. Sci. Rep. 7(1) (2017) 11600. https://doi.org/10.1038/s41598-017-11573-7.
Crossref Google Scholar
Food Science and Human Wellness
Volume 12 Issue 6,
November 2023
Pages 2369-2380
DOI: 10.1016/j.fshw.2023.03.005
Cite this article:
Hu X, Qian Y, Gao Z, et al. Safety evaluation and whole genome sequencing for revealing the ability of Penicillium oxalicum WX-209 to safely and effectively degrade citrus segments. Food Science and Human Wellness, 2023, 12(6): 2369-2380. https://doi.org/10.1016/j.fshw.2023.03.005

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Received: 03 December 2021
Revised: 05 February 2022
Accepted: 11 March 2022
Published: 04 April 2023
© 2023 Beijing Academy of Food Sciences.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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