Detecting and characterizing new endofungal bacteria in new hosts: Pandoraea sputorum and Mycetohabitans endofungorum in Rhizopus arrhizus

The fungus Rhizopus arrhizus (=R. oryzae) is commonly saprotrophic, exhibiting a nature of decomposing organic matter. Additionally, it serves as a crucial starter in food fermentation and can act as a pathogen causing mucormycosis in humans and animals. In this study, two distinct endofungal bacter...

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Main Authors: Xiao-Ling Liu, Heng Zhao, Yi-Xin Wang, Xin-Ye Liu, Yang Jiang, Meng-Fei Tao, Xiao-Yong Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1346252/full
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author Xiao-Ling Liu
Xiao-Ling Liu
Heng Zhao
Yi-Xin Wang
Xin-Ye Liu
Yang Jiang
Meng-Fei Tao
Xiao-Yong Liu
Xiao-Yong Liu
author_facet Xiao-Ling Liu
Xiao-Ling Liu
Heng Zhao
Yi-Xin Wang
Xin-Ye Liu
Yang Jiang
Meng-Fei Tao
Xiao-Yong Liu
Xiao-Yong Liu
author_sort Xiao-Ling Liu
collection DOAJ
description The fungus Rhizopus arrhizus (=R. oryzae) is commonly saprotrophic, exhibiting a nature of decomposing organic matter. Additionally, it serves as a crucial starter in food fermentation and can act as a pathogen causing mucormycosis in humans and animals. In this study, two distinct endofungal bacteria (EFBs), associated with individual strains of R. arrhizus, were identified using live/dead staining, fluorescence in situ hybridization, transmission electron microscopy, and 16S rDNA sequencing. The roles of these bacteria were elucidated through antibiotic treatment, pure cultivation, and comparative genomics. The bacterial endosymbionts, Pandoraea sputorum EFB03792 and Mycetohabitans endofungorum EFB03829, were purified from the host fungal strains R. arrhizus XY03792 and XY03829, respectively. Notably, this study marks the first report of Pandoraea as an EFB genus. Compared to its free-living counterparts, P. sputorum EFB03792 exhibited 28 specific virulence factor-related genes, six specific CE10 family genes, and 74 genes associated with type III secretion system (T3SS), emphasizing its pivotal role in invasion and colonization. Furthermore, this study introduces R. arrhizus as a new host for EFB M. endofungorum, with EFB contributing to host sporulation. Despite a visibly reduced genome, M. endofungorum EFB03829 displayed a substantial number of virulence factor-related genes, CE10 family genes, T3SS genes, mobile elements, and significant gene rearrangement. While EFBs have been previously identified in R. arrhizus, their toxin-producing potential in food fermentation has not been explored until this study. The discovery of these two new EFBs highlights their potential for toxin production within R. arrhizus, laying the groundwork for identifying suitable R. arrhizus strains for fermentation processes.
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spelling doaj.art-e8054e1d99884ba2ace88d52a41295542024-02-29T15:03:13ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-02-011510.3389/fmicb.2024.13462521346252Detecting and characterizing new endofungal bacteria in new hosts: Pandoraea sputorum and Mycetohabitans endofungorum in Rhizopus arrhizusXiao-Ling Liu0Xiao-Ling Liu1Heng Zhao2Yi-Xin Wang3Xin-Ye Liu4Yang Jiang5Meng-Fei Tao6Xiao-Yong Liu7Xiao-Yong Liu8College of Life Sciences, Shandong Normal University, Jinan, ChinaState Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Efficient Production of Forest Resources, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, ChinaCollege of Life Sciences, Shandong Normal University, Jinan, ChinaCollege of Life Sciences, Shandong Normal University, Jinan, ChinaCollege of Life Sciences, Shandong Normal University, Jinan, ChinaCollege of Life Sciences, Shandong Normal University, Jinan, ChinaCollege of Life Sciences, Shandong Normal University, Jinan, ChinaState Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaThe fungus Rhizopus arrhizus (=R. oryzae) is commonly saprotrophic, exhibiting a nature of decomposing organic matter. Additionally, it serves as a crucial starter in food fermentation and can act as a pathogen causing mucormycosis in humans and animals. In this study, two distinct endofungal bacteria (EFBs), associated with individual strains of R. arrhizus, were identified using live/dead staining, fluorescence in situ hybridization, transmission electron microscopy, and 16S rDNA sequencing. The roles of these bacteria were elucidated through antibiotic treatment, pure cultivation, and comparative genomics. The bacterial endosymbionts, Pandoraea sputorum EFB03792 and Mycetohabitans endofungorum EFB03829, were purified from the host fungal strains R. arrhizus XY03792 and XY03829, respectively. Notably, this study marks the first report of Pandoraea as an EFB genus. Compared to its free-living counterparts, P. sputorum EFB03792 exhibited 28 specific virulence factor-related genes, six specific CE10 family genes, and 74 genes associated with type III secretion system (T3SS), emphasizing its pivotal role in invasion and colonization. Furthermore, this study introduces R. arrhizus as a new host for EFB M. endofungorum, with EFB contributing to host sporulation. Despite a visibly reduced genome, M. endofungorum EFB03829 displayed a substantial number of virulence factor-related genes, CE10 family genes, T3SS genes, mobile elements, and significant gene rearrangement. While EFBs have been previously identified in R. arrhizus, their toxin-producing potential in food fermentation has not been explored until this study. The discovery of these two new EFBs highlights their potential for toxin production within R. arrhizus, laying the groundwork for identifying suitable R. arrhizus strains for fermentation processes.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1346252/fullRhizopus oryzaenovel endosymbiontendohyphal bacteriumPandoraea sputorumcomparative genomics
spellingShingle Xiao-Ling Liu
Xiao-Ling Liu
Heng Zhao
Yi-Xin Wang
Xin-Ye Liu
Yang Jiang
Meng-Fei Tao
Xiao-Yong Liu
Xiao-Yong Liu
Detecting and characterizing new endofungal bacteria in new hosts: Pandoraea sputorum and Mycetohabitans endofungorum in Rhizopus arrhizus
Frontiers in Microbiology
Rhizopus oryzae
novel endosymbiont
endohyphal bacterium
Pandoraea sputorum
comparative genomics
title Detecting and characterizing new endofungal bacteria in new hosts: Pandoraea sputorum and Mycetohabitans endofungorum in Rhizopus arrhizus
title_full Detecting and characterizing new endofungal bacteria in new hosts: Pandoraea sputorum and Mycetohabitans endofungorum in Rhizopus arrhizus
title_fullStr Detecting and characterizing new endofungal bacteria in new hosts: Pandoraea sputorum and Mycetohabitans endofungorum in Rhizopus arrhizus
title_full_unstemmed Detecting and characterizing new endofungal bacteria in new hosts: Pandoraea sputorum and Mycetohabitans endofungorum in Rhizopus arrhizus
title_short Detecting and characterizing new endofungal bacteria in new hosts: Pandoraea sputorum and Mycetohabitans endofungorum in Rhizopus arrhizus
title_sort detecting and characterizing new endofungal bacteria in new hosts pandoraea sputorum and mycetohabitans endofungorum in rhizopus arrhizus
topic Rhizopus oryzae
novel endosymbiont
endohyphal bacterium
Pandoraea sputorum
comparative genomics
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1346252/full
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