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Genome sequencing and identification of cellulase genes in Bacillus paralicheniformis strains from the Red Sea

BACKGROUND: Cellulolytic microorganisms are considered a key player in the degradation of plant biomass in various environments. These microorganisms can be isolated from various environments, such as soils, the insect gut, the mammalian rumen and oceans. The Red Sea exhibits a unique environment in...

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Autores principales: Fatani, Siham, Saito, Yoshimoto, Alarawi, Mohammed, Gojobori, Takashi, Mineta, Katsuhiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8456639/
https://www.ncbi.nlm.nih.gov/pubmed/34548024
http://dx.doi.org/10.1186/s12866-021-02316-w
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author Fatani, Siham
Saito, Yoshimoto
Alarawi, Mohammed
Gojobori, Takashi
Mineta, Katsuhiko
author_facet Fatani, Siham
Saito, Yoshimoto
Alarawi, Mohammed
Gojobori, Takashi
Mineta, Katsuhiko
author_sort Fatani, Siham
collection PubMed
description BACKGROUND: Cellulolytic microorganisms are considered a key player in the degradation of plant biomass in various environments. These microorganisms can be isolated from various environments, such as soils, the insect gut, the mammalian rumen and oceans. The Red Sea exhibits a unique environment in terms of presenting a high seawater temperature, high salinity, low nutrient levels and high biodiversity. However, there is little information regarding cellulase genes in the Red Sea environment. This study aimed to examine whether the Red Sea can be a resource for the bioprospecting of microbial cellulases by isolating cellulase-producing microorganisms from the Red Sea environment and characterizing cellulase genes. RESULTS: Three bacterial strains were successfully isolated from the plankton fraction and the surface of seagrass. The isolated strains were identified as Bacillus paralicheniformis and showed strong cellulase activity. These results suggested that these three isolates secreted active cellulases. By whole genome sequencing, we found 10 cellulase genes from the three isolates. We compared the expression of these cellulase genes under cellulase-inducing and non-inducing conditions and found that most of the cellulase genes were generally upregulated during cellulolysis in the isolates. Our operon structure analysis also showed that cellulase genes form operons with genes involved in various kinds of cellular reactions, such as protein metabolism, which suggests the existence of crosstalk between cellulolysis and other metabolic pathways in the bacterial isolates. These results suggest that multiple cellulases are playing important roles in cellulolysis. CONCLUSIONS: Our study reports the isolation and characterization of cellulase-producing bacteria from the Red Sea. Our whole-genome sequencing classified our three isolates as Bacillus paralicheniformis, and we revealed the presence of ten cellulase orthologues in each of three isolates’ genomes. Our comparative expression analysis also identified that most of the cellulase genes were upregulated under the inducing conditions in general. Although cellulases have been roughly classified into three enzyme groups of beta-glucosidase, endo-β-1,4-glucanase and exoglucanase, these findings suggest the importance to consider microbial cellulolysis as a more complex reaction with various kinds of cellulase enzymes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-021-02316-w.
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spelling pubmed-84566392021-09-22 Genome sequencing and identification of cellulase genes in Bacillus paralicheniformis strains from the Red Sea Fatani, Siham Saito, Yoshimoto Alarawi, Mohammed Gojobori, Takashi Mineta, Katsuhiko BMC Microbiol Research BACKGROUND: Cellulolytic microorganisms are considered a key player in the degradation of plant biomass in various environments. These microorganisms can be isolated from various environments, such as soils, the insect gut, the mammalian rumen and oceans. The Red Sea exhibits a unique environment in terms of presenting a high seawater temperature, high salinity, low nutrient levels and high biodiversity. However, there is little information regarding cellulase genes in the Red Sea environment. This study aimed to examine whether the Red Sea can be a resource for the bioprospecting of microbial cellulases by isolating cellulase-producing microorganisms from the Red Sea environment and characterizing cellulase genes. RESULTS: Three bacterial strains were successfully isolated from the plankton fraction and the surface of seagrass. The isolated strains were identified as Bacillus paralicheniformis and showed strong cellulase activity. These results suggested that these three isolates secreted active cellulases. By whole genome sequencing, we found 10 cellulase genes from the three isolates. We compared the expression of these cellulase genes under cellulase-inducing and non-inducing conditions and found that most of the cellulase genes were generally upregulated during cellulolysis in the isolates. Our operon structure analysis also showed that cellulase genes form operons with genes involved in various kinds of cellular reactions, such as protein metabolism, which suggests the existence of crosstalk between cellulolysis and other metabolic pathways in the bacterial isolates. These results suggest that multiple cellulases are playing important roles in cellulolysis. CONCLUSIONS: Our study reports the isolation and characterization of cellulase-producing bacteria from the Red Sea. Our whole-genome sequencing classified our three isolates as Bacillus paralicheniformis, and we revealed the presence of ten cellulase orthologues in each of three isolates’ genomes. Our comparative expression analysis also identified that most of the cellulase genes were upregulated under the inducing conditions in general. Although cellulases have been roughly classified into three enzyme groups of beta-glucosidase, endo-β-1,4-glucanase and exoglucanase, these findings suggest the importance to consider microbial cellulolysis as a more complex reaction with various kinds of cellulase enzymes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-021-02316-w. BioMed Central 2021-09-22 /pmc/articles/PMC8456639/ /pubmed/34548024 http://dx.doi.org/10.1186/s12866-021-02316-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Fatani, Siham
Saito, Yoshimoto
Alarawi, Mohammed
Gojobori, Takashi
Mineta, Katsuhiko
Genome sequencing and identification of cellulase genes in Bacillus paralicheniformis strains from the Red Sea
title Genome sequencing and identification of cellulase genes in Bacillus paralicheniformis strains from the Red Sea
title_full Genome sequencing and identification of cellulase genes in Bacillus paralicheniformis strains from the Red Sea
title_fullStr Genome sequencing and identification of cellulase genes in Bacillus paralicheniformis strains from the Red Sea
title_full_unstemmed Genome sequencing and identification of cellulase genes in Bacillus paralicheniformis strains from the Red Sea
title_short Genome sequencing and identification of cellulase genes in Bacillus paralicheniformis strains from the Red Sea
title_sort genome sequencing and identification of cellulase genes in bacillus paralicheniformis strains from the red sea
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8456639/
https://www.ncbi.nlm.nih.gov/pubmed/34548024
http://dx.doi.org/10.1186/s12866-021-02316-w
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