Endosymbiotic bacteria within the nematode-trapping fungus Arthrobotrys musiformis and their potential roles in nitrogen cycling

Endosymbiotic bacteria (ESB) have important effects on their hosts, contributing to its growth, reproduction and biological functions. Although the effects of exogenous bacteria on the trap formation of nematode-trapping fungi (NTF) have been revealed, the effects of ESB on NTF remain unknown. In th...

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Main Authors: Hua Zheng, Tong Chen, Wenjie Li, Jianan Hong, Jianping Xu, Zefen Yu
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1349447/full
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author Hua Zheng
Hua Zheng
Tong Chen
Tong Chen
Wenjie Li
Wenjie Li
Jianan Hong
Jianan Hong
Jianping Xu
Zefen Yu
author_facet Hua Zheng
Hua Zheng
Tong Chen
Tong Chen
Wenjie Li
Wenjie Li
Jianan Hong
Jianan Hong
Jianping Xu
Zefen Yu
author_sort Hua Zheng
collection DOAJ
description Endosymbiotic bacteria (ESB) have important effects on their hosts, contributing to its growth, reproduction and biological functions. Although the effects of exogenous bacteria on the trap formation of nematode-trapping fungi (NTF) have been revealed, the effects of ESB on NTF remain unknown. In this study, we investigated the species diversity of ESB in the NTF Arthrobotrys musiformis using high-throughput sequencing and culture-dependent approaches, and compared bacterial profiles to assess the effects of strain source and culture media on A. musiformis. PICRUSt2 and FAPROTAX were used to predict bacterial function. Our study revealed that bacterial communities in A. musiformis displayed high diversity and heterogeneity, with Proteobacteria, Firmicutes, Bacteroidetes and Actinobacteria as the dominant phyla. The ESB between A. musiformis groups isolated from different habitats and cultured in the same medium were more similar to each other than the other groups isolated from the same habitat but cultured in different media. Function analysis predicted a broad and diverse functional repertoire of ESB in A. musiformis, and unveiled that ESB have the potential to function in five modules of the nitrogen metabolism. We isolated nitrogen-fixing and denitrifying bacteria from the ESB and demonstrated their effects on trap formation of A. musiformis. Among seven bacteria that we tested, three bacterial species Bacillus licheniformis, Achromobacter xylosoxidans and Stenotrophomonas maltophilia were found to be efficient in inducing trap formation. In conclusion, this study revealed extensive ESB diversity within NTF and demonstrated that these bacteria likely play important roles in nitrogen cycling, including nematode trap formation.
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spelling doaj.art-619989e3f4f44f89b2311da21b3481222024-01-29T17:36:02ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-01-011510.3389/fmicb.2024.13494471349447Endosymbiotic bacteria within the nematode-trapping fungus Arthrobotrys musiformis and their potential roles in nitrogen cyclingHua Zheng0Hua Zheng1Tong Chen2Tong Chen3Wenjie Li4Wenjie Li5Jianan Hong6Jianan Hong7Jianping Xu8Zefen Yu9Laboratory for Conservation and Utilization of Bio-Resources, Yunnan University, Kunming, ChinaSchool of Life Sciences, Yunnan University, Kunming, ChinaLaboratory for Conservation and Utilization of Bio-Resources, Yunnan University, Kunming, ChinaSchool of Life Sciences, Yunnan University, Kunming, ChinaLaboratory for Conservation and Utilization of Bio-Resources, Yunnan University, Kunming, ChinaSchool of Life Sciences, Yunnan University, Kunming, ChinaLaboratory for Conservation and Utilization of Bio-Resources, Yunnan University, Kunming, ChinaSchool of Life Sciences, Yunnan University, Kunming, ChinaDepartment of Biology, McMaster University, Hamilton, ON, CanadaLaboratory for Conservation and Utilization of Bio-Resources, Yunnan University, Kunming, ChinaEndosymbiotic bacteria (ESB) have important effects on their hosts, contributing to its growth, reproduction and biological functions. Although the effects of exogenous bacteria on the trap formation of nematode-trapping fungi (NTF) have been revealed, the effects of ESB on NTF remain unknown. In this study, we investigated the species diversity of ESB in the NTF Arthrobotrys musiformis using high-throughput sequencing and culture-dependent approaches, and compared bacterial profiles to assess the effects of strain source and culture media on A. musiformis. PICRUSt2 and FAPROTAX were used to predict bacterial function. Our study revealed that bacterial communities in A. musiformis displayed high diversity and heterogeneity, with Proteobacteria, Firmicutes, Bacteroidetes and Actinobacteria as the dominant phyla. The ESB between A. musiformis groups isolated from different habitats and cultured in the same medium were more similar to each other than the other groups isolated from the same habitat but cultured in different media. Function analysis predicted a broad and diverse functional repertoire of ESB in A. musiformis, and unveiled that ESB have the potential to function in five modules of the nitrogen metabolism. We isolated nitrogen-fixing and denitrifying bacteria from the ESB and demonstrated their effects on trap formation of A. musiformis. Among seven bacteria that we tested, three bacterial species Bacillus licheniformis, Achromobacter xylosoxidans and Stenotrophomonas maltophilia were found to be efficient in inducing trap formation. In conclusion, this study revealed extensive ESB diversity within NTF and demonstrated that these bacteria likely play important roles in nitrogen cycling, including nematode trap formation.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1349447/fullnematode-trapping fungiendosymbiosisbacterial diversitynitrogen metabolismnitrogen-fixing bacteriadenitrifying bacteria
spellingShingle Hua Zheng
Hua Zheng
Tong Chen
Tong Chen
Wenjie Li
Wenjie Li
Jianan Hong
Jianan Hong
Jianping Xu
Zefen Yu
Endosymbiotic bacteria within the nematode-trapping fungus Arthrobotrys musiformis and their potential roles in nitrogen cycling
Frontiers in Microbiology
nematode-trapping fungi
endosymbiosis
bacterial diversity
nitrogen metabolism
nitrogen-fixing bacteria
denitrifying bacteria
title Endosymbiotic bacteria within the nematode-trapping fungus Arthrobotrys musiformis and their potential roles in nitrogen cycling
title_full Endosymbiotic bacteria within the nematode-trapping fungus Arthrobotrys musiformis and their potential roles in nitrogen cycling
title_fullStr Endosymbiotic bacteria within the nematode-trapping fungus Arthrobotrys musiformis and their potential roles in nitrogen cycling
title_full_unstemmed Endosymbiotic bacteria within the nematode-trapping fungus Arthrobotrys musiformis and their potential roles in nitrogen cycling
title_short Endosymbiotic bacteria within the nematode-trapping fungus Arthrobotrys musiformis and their potential roles in nitrogen cycling
title_sort endosymbiotic bacteria within the nematode trapping fungus arthrobotrys musiformis and their potential roles in nitrogen cycling
topic nematode-trapping fungi
endosymbiosis
bacterial diversity
nitrogen metabolism
nitrogen-fixing bacteria
denitrifying bacteria
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1349447/full
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