Cargando…

Insight into the phylogeny and metabolic divergence of Monascus species (M. pilosus, M. ruber, and M. purpureus) at the genome level

BACKGROUND: Species of the genus Monascus are economically important and widely used in the production of food colorants and monacolin K. However, they have also been known to produce the mycotoxin citrinin. Currently, taxonomic knowledge of this species at the genome level is insufficient. METHODS:...

Descripción completa

Detalles Bibliográficos
Autores principales: Zhang, Zhiyu, Cui, Mengfei, Chen, Panting, Li, Juxing, Mao, Zhitao, Mao, Yufeng, Li, Zhenjing, Guo, Qingbin, Wang, Changlu, Liao, Xiaoping, Liu, Huanhuan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10249731/
https://www.ncbi.nlm.nih.gov/pubmed/37303795
http://dx.doi.org/10.3389/fmicb.2023.1199144
_version_ 1785055612227289088
author Zhang, Zhiyu
Cui, Mengfei
Chen, Panting
Li, Juxing
Mao, Zhitao
Mao, Yufeng
Li, Zhenjing
Guo, Qingbin
Wang, Changlu
Liao, Xiaoping
Liu, Huanhuan
author_facet Zhang, Zhiyu
Cui, Mengfei
Chen, Panting
Li, Juxing
Mao, Zhitao
Mao, Yufeng
Li, Zhenjing
Guo, Qingbin
Wang, Changlu
Liao, Xiaoping
Liu, Huanhuan
author_sort Zhang, Zhiyu
collection PubMed
description BACKGROUND: Species of the genus Monascus are economically important and widely used in the production of food colorants and monacolin K. However, they have also been known to produce the mycotoxin citrinin. Currently, taxonomic knowledge of this species at the genome level is insufficient. METHODS: This study presents genomic similarity analyses through the analysis of the average nucleic acid identity of the genomic sequence and the whole genome alignment. Subsequently, the study constructed a pangenome of Monascus by reannotating all the genomes and identifying a total of 9,539 orthologous gene families. Two phylogenetic trees were constructed based on 4,589 single copy orthologous protein sequences and all the 5,565 orthologous proteins, respectively. In addition, carbohydrate active enzymes, secretome, allergic proteins, as well as secondary metabolite gene clusters were compared among the included 15 Monascus strains. RESULTS: The results clearly revealed a high homology between M. pilosus and M. ruber, and their distant relationship with M. purpureus. Accordingly, all the included 15 Monascus strains should be classified into two distinctly evolutionary clades, namely the M. purpureus clade and the M. pilosus-M. ruber clade. Moreover, gene ontology enrichment showed that the M. pilosus-M. ruber clade had more orthologous genes involved with environmental adaptation than the M. purpureus clade. Compared to Aspergillus oryzae, all the Monascus species had a substantial gene loss of carbohydrate active enzymes. Potential allergenic and fungal virulence factor proteins were also found in the secretome of Monascus. Furthermore, this study identified the pigment synthesis gene clusters present in all included genomes, but with multiple nonessential genes inserted in the gene cluster of M. pilosus and M. ruber compared to M. purpureus. The citrinin gene cluster was found to be intact and highly conserved only among M. purpureus genomes. The monacolin K gene cluster was found only in the genomes of M. pilosus and M. ruber, but the sequence was more conserved in M. ruber. CONCLUSION: This study provides a paradigm for phylogenetic analysis of the genus Monascus, and it is believed that this report will lead to a better understanding of these food microorganisms in terms of classification, metabolic differentiation, and safety.
format Online
Article
Text
id pubmed-10249731
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-102497312023-06-09 Insight into the phylogeny and metabolic divergence of Monascus species (M. pilosus, M. ruber, and M. purpureus) at the genome level Zhang, Zhiyu Cui, Mengfei Chen, Panting Li, Juxing Mao, Zhitao Mao, Yufeng Li, Zhenjing Guo, Qingbin Wang, Changlu Liao, Xiaoping Liu, Huanhuan Front Microbiol Microbiology BACKGROUND: Species of the genus Monascus are economically important and widely used in the production of food colorants and monacolin K. However, they have also been known to produce the mycotoxin citrinin. Currently, taxonomic knowledge of this species at the genome level is insufficient. METHODS: This study presents genomic similarity analyses through the analysis of the average nucleic acid identity of the genomic sequence and the whole genome alignment. Subsequently, the study constructed a pangenome of Monascus by reannotating all the genomes and identifying a total of 9,539 orthologous gene families. Two phylogenetic trees were constructed based on 4,589 single copy orthologous protein sequences and all the 5,565 orthologous proteins, respectively. In addition, carbohydrate active enzymes, secretome, allergic proteins, as well as secondary metabolite gene clusters were compared among the included 15 Monascus strains. RESULTS: The results clearly revealed a high homology between M. pilosus and M. ruber, and their distant relationship with M. purpureus. Accordingly, all the included 15 Monascus strains should be classified into two distinctly evolutionary clades, namely the M. purpureus clade and the M. pilosus-M. ruber clade. Moreover, gene ontology enrichment showed that the M. pilosus-M. ruber clade had more orthologous genes involved with environmental adaptation than the M. purpureus clade. Compared to Aspergillus oryzae, all the Monascus species had a substantial gene loss of carbohydrate active enzymes. Potential allergenic and fungal virulence factor proteins were also found in the secretome of Monascus. Furthermore, this study identified the pigment synthesis gene clusters present in all included genomes, but with multiple nonessential genes inserted in the gene cluster of M. pilosus and M. ruber compared to M. purpureus. The citrinin gene cluster was found to be intact and highly conserved only among M. purpureus genomes. The monacolin K gene cluster was found only in the genomes of M. pilosus and M. ruber, but the sequence was more conserved in M. ruber. CONCLUSION: This study provides a paradigm for phylogenetic analysis of the genus Monascus, and it is believed that this report will lead to a better understanding of these food microorganisms in terms of classification, metabolic differentiation, and safety. Frontiers Media S.A. 2023-05-25 /pmc/articles/PMC10249731/ /pubmed/37303795 http://dx.doi.org/10.3389/fmicb.2023.1199144 Text en Copyright © 2023 Zhang, Cui, Chen, Li, Mao, Mao, Li, Guo, Wang, Liao and Liu. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Zhang, Zhiyu
Cui, Mengfei
Chen, Panting
Li, Juxing
Mao, Zhitao
Mao, Yufeng
Li, Zhenjing
Guo, Qingbin
Wang, Changlu
Liao, Xiaoping
Liu, Huanhuan
Insight into the phylogeny and metabolic divergence of Monascus species (M. pilosus, M. ruber, and M. purpureus) at the genome level
title Insight into the phylogeny and metabolic divergence of Monascus species (M. pilosus, M. ruber, and M. purpureus) at the genome level
title_full Insight into the phylogeny and metabolic divergence of Monascus species (M. pilosus, M. ruber, and M. purpureus) at the genome level
title_fullStr Insight into the phylogeny and metabolic divergence of Monascus species (M. pilosus, M. ruber, and M. purpureus) at the genome level
title_full_unstemmed Insight into the phylogeny and metabolic divergence of Monascus species (M. pilosus, M. ruber, and M. purpureus) at the genome level
title_short Insight into the phylogeny and metabolic divergence of Monascus species (M. pilosus, M. ruber, and M. purpureus) at the genome level
title_sort insight into the phylogeny and metabolic divergence of monascus species (m. pilosus, m. ruber, and m. purpureus) at the genome level
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10249731/
https://www.ncbi.nlm.nih.gov/pubmed/37303795
http://dx.doi.org/10.3389/fmicb.2023.1199144
work_keys_str_mv AT zhangzhiyu insightintothephylogenyandmetabolicdivergenceofmonascusspeciesmpilosusmruberandmpurpureusatthegenomelevel
AT cuimengfei insightintothephylogenyandmetabolicdivergenceofmonascusspeciesmpilosusmruberandmpurpureusatthegenomelevel
AT chenpanting insightintothephylogenyandmetabolicdivergenceofmonascusspeciesmpilosusmruberandmpurpureusatthegenomelevel
AT lijuxing insightintothephylogenyandmetabolicdivergenceofmonascusspeciesmpilosusmruberandmpurpureusatthegenomelevel
AT maozhitao insightintothephylogenyandmetabolicdivergenceofmonascusspeciesmpilosusmruberandmpurpureusatthegenomelevel
AT maoyufeng insightintothephylogenyandmetabolicdivergenceofmonascusspeciesmpilosusmruberandmpurpureusatthegenomelevel
AT lizhenjing insightintothephylogenyandmetabolicdivergenceofmonascusspeciesmpilosusmruberandmpurpureusatthegenomelevel
AT guoqingbin insightintothephylogenyandmetabolicdivergenceofmonascusspeciesmpilosusmruberandmpurpureusatthegenomelevel
AT wangchanglu insightintothephylogenyandmetabolicdivergenceofmonascusspeciesmpilosusmruberandmpurpureusatthegenomelevel
AT liaoxiaoping insightintothephylogenyandmetabolicdivergenceofmonascusspeciesmpilosusmruberandmpurpureusatthegenomelevel
AT liuhuanhuan insightintothephylogenyandmetabolicdivergenceofmonascusspeciesmpilosusmruberandmpurpureusatthegenomelevel