Characterization of a Deep Sea Bacillus toyonensis Isolate: Genomic and Pathogenic Features

Bacillus toyonensis is a group of Gram-positive bacteria belonging to the Bacillus cereus group and used in some cases as probiotics or biocontrol agents. To our knowledge, B. toyonensis from the deep sea (depth >1,000 m) has not been documented. Here, we report the isolation and characteriza...

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Main Authors: Jing-chang Luo, Hao Long, Jian Zhang, Yan Zhao, Li Sun
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2021.629116/full
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spelling doaj-bd15b2d3fb3c40b588f539abe65235aa2021-03-10T06:26:45ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882021-03-011110.3389/fcimb.2021.629116629116Characterization of a Deep Sea Bacillus toyonensis Isolate: Genomic and Pathogenic FeaturesJing-chang Luo0Jing-chang Luo1Jing-chang Luo2Hao Long3Jian Zhang4Yan Zhao5Yan Zhao6Li Sun7Li Sun8Li Sun9CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology, Qingdao, ChinaCollege of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, ChinaSchool of Ocean, Yan Tai University, Yantai, ChinaCAS and Shandong Province Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology, Qingdao, ChinaCAS and Shandong Province Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology, Qingdao, ChinaCollege of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing, ChinaBacillus toyonensis is a group of Gram-positive bacteria belonging to the Bacillus cereus group and used in some cases as probiotics or biocontrol agents. To our knowledge, B. toyonensis from the deep sea (depth >1,000 m) has not been documented. Here, we report the isolation and characterization of a B. toyonensis strain, P18, from a deep sea hydrothermal field. P18 is aerobic, motile, and able to grow at low temperatures (4°C) and high concentrations of NaCl (8%). P18 possesses a circular chromosome of 5,250,895 bp and a plasmid of 536,892 bp, which encode 5,380 and 523 genes, respectively. Of these genes, 2,229 encode hypothetical proteins that could not be annotated based on the COG database. Comparative genomic analysis showed that P18 is most closely related to the type strain of B. toyonensis, BCT-7112T. Compared to BCT-7112T, P18 contains 1,401 unique genes, 441 of which were classified into 20 COG functional categories, and the remaining 960 genes could not be annotated. A total of 319 putative virulence genes were identified in P18, including toxin-related genes, and 24 of these genes are absent in BCT-7112T. P18 exerted strong cytopathic effects on fish and mammalian cells that led to rapid cell death. When inoculated via injection into fish and mice, P18 rapidly disseminated in host tissues and induced acute infection and mortality. Histopathology revealed varying degrees of tissue lesions in the infected animals. Furthermore, P18 could survive in fish and mouse sera and possessed hemolytic activity. Taken together, these results provide the first evidence that virulent B. toyonensis exists in deep sea environments.https://www.frontiersin.org/articles/10.3389/fcimb.2021.629116/fullBacillus toyonensisdeep-sea hydrothermal ventvirulenceinfectiongenome
collection DOAJ
language English
format Article
sources DOAJ
author Jing-chang Luo
Jing-chang Luo
Jing-chang Luo
Hao Long
Jian Zhang
Yan Zhao
Yan Zhao
Li Sun
Li Sun
Li Sun
spellingShingle Jing-chang Luo
Jing-chang Luo
Jing-chang Luo
Hao Long
Jian Zhang
Yan Zhao
Yan Zhao
Li Sun
Li Sun
Li Sun
Characterization of a Deep Sea Bacillus toyonensis Isolate: Genomic and Pathogenic Features
Frontiers in Cellular and Infection Microbiology
Bacillus toyonensis
deep-sea hydrothermal vent
virulence
infection
genome
author_facet Jing-chang Luo
Jing-chang Luo
Jing-chang Luo
Hao Long
Jian Zhang
Yan Zhao
Yan Zhao
Li Sun
Li Sun
Li Sun
author_sort Jing-chang Luo
title Characterization of a Deep Sea Bacillus toyonensis Isolate: Genomic and Pathogenic Features
title_short Characterization of a Deep Sea Bacillus toyonensis Isolate: Genomic and Pathogenic Features
title_full Characterization of a Deep Sea Bacillus toyonensis Isolate: Genomic and Pathogenic Features
title_fullStr Characterization of a Deep Sea Bacillus toyonensis Isolate: Genomic and Pathogenic Features
title_full_unstemmed Characterization of a Deep Sea Bacillus toyonensis Isolate: Genomic and Pathogenic Features
title_sort characterization of a deep sea bacillus toyonensis isolate: genomic and pathogenic features
publisher Frontiers Media S.A.
series Frontiers in Cellular and Infection Microbiology
issn 2235-2988
publishDate 2021-03-01
description Bacillus toyonensis is a group of Gram-positive bacteria belonging to the Bacillus cereus group and used in some cases as probiotics or biocontrol agents. To our knowledge, B. toyonensis from the deep sea (depth >1,000 m) has not been documented. Here, we report the isolation and characterization of a B. toyonensis strain, P18, from a deep sea hydrothermal field. P18 is aerobic, motile, and able to grow at low temperatures (4°C) and high concentrations of NaCl (8%). P18 possesses a circular chromosome of 5,250,895 bp and a plasmid of 536,892 bp, which encode 5,380 and 523 genes, respectively. Of these genes, 2,229 encode hypothetical proteins that could not be annotated based on the COG database. Comparative genomic analysis showed that P18 is most closely related to the type strain of B. toyonensis, BCT-7112T. Compared to BCT-7112T, P18 contains 1,401 unique genes, 441 of which were classified into 20 COG functional categories, and the remaining 960 genes could not be annotated. A total of 319 putative virulence genes were identified in P18, including toxin-related genes, and 24 of these genes are absent in BCT-7112T. P18 exerted strong cytopathic effects on fish and mammalian cells that led to rapid cell death. When inoculated via injection into fish and mice, P18 rapidly disseminated in host tissues and induced acute infection and mortality. Histopathology revealed varying degrees of tissue lesions in the infected animals. Furthermore, P18 could survive in fish and mouse sera and possessed hemolytic activity. Taken together, these results provide the first evidence that virulent B. toyonensis exists in deep sea environments.
topic Bacillus toyonensis
deep-sea hydrothermal vent
virulence
infection
genome
url https://www.frontiersin.org/articles/10.3389/fcimb.2021.629116/full
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