AUTHOR=Zhang Zhiyu , Cui Mengfei , Chen Panting , Li Juxing , Mao Zhitao , Mao Yufeng , Li Zhenjing , Guo Qingbin , Wang Changlu , Liao Xiaoping , Liu Huanhuan 

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

JOURNAL=Frontiers in Microbiology

VOLUME=14

YEAR=2023

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2023.1199144

DOI=10.3389/fmicb.2023.1199144

ISSN=1664-302X

ABSTRACT=<sec><title>Background</title><p>Species of the genus <italic>Monascus</italic> 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.</p></sec><sec><title>Methods</title><p>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 <italic>Monascus</italic> 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 <italic>Monascus</italic> strains.</p></sec><sec><title>Results</title><p>The results clearly revealed a high homology between <italic>M. pilosus</italic> and <italic>M. ruber</italic>, and their distant relationship with <italic>M. purpureus</italic>. Accordingly, all the included 15 <italic>Monascus</italic> strains should be classified into two distinctly evolutionary clades, namely the <italic>M. purpureus</italic> clade and the <italic>M. pilosus</italic>-<italic>M. ruber</italic> clade. Moreover, gene ontology enrichment showed that the <italic>M. pilosus</italic>-<italic>M. ruber</italic> clade had more orthologous genes involved with environmental adaptation than the <italic>M. purpureus</italic> clade. Compared to <italic>Aspergillus oryzae</italic>, all the <italic>Monascus</italic> species had a substantial gene loss of carbohydrate active enzymes. Potential allergenic and fungal virulence factor proteins were also found in the secretome of <italic>Monascus</italic>. 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 <italic>M. pilosus</italic> and <italic>M. ruber</italic> compared to <italic>M. purpureus</italic>. The citrinin gene cluster was found to be intact and highly conserved only among <italic>M. purpureus</italic> genomes. The monacolin K gene cluster was found only in the genomes of <italic>M. pilosus</italic> and <italic>M. ruber</italic>, but the sequence was more conserved in <italic>M. ruber.</italic></p></sec><sec><title>Conclusion</title><p>This study provides a paradigm for phylogenetic analysis of the genus <italic>Monascus</italic>, 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.</p></sec>