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Delving into the lifestyle of Sundarban Wetland resident, biofilm producing, halotolerant Salinicoccus roseus: a comparative genomics-based intervention

BACKGROUND: Microbial community played an essential role in ecosystem processes, be it mangrove wetland or other intertidal ecologies. Several enzymatic activities like hydrolases are effective ecological indicators of soil microbial function. So far, little is known on halophilic bacterial contribu...

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Autores principales: Dutta, Bhramar, Halder, Urmi, Chitikineni, Annapurna, Varshney, Rajeev K., Bandopadhyay, Rajib
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10642018/
https://www.ncbi.nlm.nih.gov/pubmed/37957573
http://dx.doi.org/10.1186/s12864-023-09764-w
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author Dutta, Bhramar
Halder, Urmi
Chitikineni, Annapurna
Varshney, Rajeev K.
Bandopadhyay, Rajib
author_facet Dutta, Bhramar
Halder, Urmi
Chitikineni, Annapurna
Varshney, Rajeev K.
Bandopadhyay, Rajib
author_sort Dutta, Bhramar
collection PubMed
description BACKGROUND: Microbial community played an essential role in ecosystem processes, be it mangrove wetland or other intertidal ecologies. Several enzymatic activities like hydrolases are effective ecological indicators of soil microbial function. So far, little is known on halophilic bacterial contribution and function on a genomic viewpoint of Indian Sundarban Wetland. Considering the above mentioned issues, the aims of this study was to understand the life style, metabolic functionalities and genomic features of the isolated bacterium, Salinicoccus roseus strain RF1H. A comparative genome-based study of S. roseus has not been reported yet. Henceforth, we have considered the inclusion of the intra-species genome comparison of S. roseus to gain insight into the high degree of variation in the genome of strain RF1H among others. RESULTS: Salinicoccus roseus strain RF1H is a pink-red pigmented, Gram-positive and non-motile cocci. The bacterium exhibited high salt tolerance (up to 15% NaCl), antibiotic resistance, biofilm formation and secretion of extracellular hydrolytic enzymes. The circular genome was approximately 2.62978 Mb in size, encoding 574 predicted genes with GC content 49.5%. Presence of genomic elements (prophages, transposable elements, CRISPR-Cas system) represented bacterial virulence and multidrug-resistance. Furthermore, genes associated with salt tolerance, temperature adaptation and DNA repair system were distributed in 17 genomic islands. Genes related to hydrocarbon degradation manifested metabolic capability of the bacterium for potential biotechnological applications. A comparative pangenome analysis revealed two-component response regulator, modified C4-dicarboxylate transport system and osmotic stress regulated ATP-binding proteins. Presence of genes encoding arginine decarboxylase (ADC) enzyme being involved in biofilm formation was reported from the genome. In silico study revealed the protein is thermostable and made up with ~ 415 amino acids, and hydrophilic in nature. Three motifs appeared to be evolutionary conserved in all Salinicoccus sequences. CONCLUSION: The first report of whole genome analysis of Salinicoccus roseus strain RF1H provided information of metabolic functionalities, biofilm formation, resistance mechanism and adaptation strategies to thrive in climate-change induced vulnerable spot like Sundarban. Comparative genome analysis highlighted the unique genome content that contributed the strain’s adaptability. The biomolecules produced during metabolism are important sources of compounds with potential beneficial applications in pharmaceuticals. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09764-w.
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spelling pubmed-106420182023-11-14 Delving into the lifestyle of Sundarban Wetland resident, biofilm producing, halotolerant Salinicoccus roseus: a comparative genomics-based intervention Dutta, Bhramar Halder, Urmi Chitikineni, Annapurna Varshney, Rajeev K. Bandopadhyay, Rajib BMC Genomics Research BACKGROUND: Microbial community played an essential role in ecosystem processes, be it mangrove wetland or other intertidal ecologies. Several enzymatic activities like hydrolases are effective ecological indicators of soil microbial function. So far, little is known on halophilic bacterial contribution and function on a genomic viewpoint of Indian Sundarban Wetland. Considering the above mentioned issues, the aims of this study was to understand the life style, metabolic functionalities and genomic features of the isolated bacterium, Salinicoccus roseus strain RF1H. A comparative genome-based study of S. roseus has not been reported yet. Henceforth, we have considered the inclusion of the intra-species genome comparison of S. roseus to gain insight into the high degree of variation in the genome of strain RF1H among others. RESULTS: Salinicoccus roseus strain RF1H is a pink-red pigmented, Gram-positive and non-motile cocci. The bacterium exhibited high salt tolerance (up to 15% NaCl), antibiotic resistance, biofilm formation and secretion of extracellular hydrolytic enzymes. The circular genome was approximately 2.62978 Mb in size, encoding 574 predicted genes with GC content 49.5%. Presence of genomic elements (prophages, transposable elements, CRISPR-Cas system) represented bacterial virulence and multidrug-resistance. Furthermore, genes associated with salt tolerance, temperature adaptation and DNA repair system were distributed in 17 genomic islands. Genes related to hydrocarbon degradation manifested metabolic capability of the bacterium for potential biotechnological applications. A comparative pangenome analysis revealed two-component response regulator, modified C4-dicarboxylate transport system and osmotic stress regulated ATP-binding proteins. Presence of genes encoding arginine decarboxylase (ADC) enzyme being involved in biofilm formation was reported from the genome. In silico study revealed the protein is thermostable and made up with ~ 415 amino acids, and hydrophilic in nature. Three motifs appeared to be evolutionary conserved in all Salinicoccus sequences. CONCLUSION: The first report of whole genome analysis of Salinicoccus roseus strain RF1H provided information of metabolic functionalities, biofilm formation, resistance mechanism and adaptation strategies to thrive in climate-change induced vulnerable spot like Sundarban. Comparative genome analysis highlighted the unique genome content that contributed the strain’s adaptability. The biomolecules produced during metabolism are important sources of compounds with potential beneficial applications in pharmaceuticals. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09764-w. BioMed Central 2023-11-13 /pmc/articles/PMC10642018/ /pubmed/37957573 http://dx.doi.org/10.1186/s12864-023-09764-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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
Dutta, Bhramar
Halder, Urmi
Chitikineni, Annapurna
Varshney, Rajeev K.
Bandopadhyay, Rajib
Delving into the lifestyle of Sundarban Wetland resident, biofilm producing, halotolerant Salinicoccus roseus: a comparative genomics-based intervention
title Delving into the lifestyle of Sundarban Wetland resident, biofilm producing, halotolerant Salinicoccus roseus: a comparative genomics-based intervention
title_full Delving into the lifestyle of Sundarban Wetland resident, biofilm producing, halotolerant Salinicoccus roseus: a comparative genomics-based intervention
title_fullStr Delving into the lifestyle of Sundarban Wetland resident, biofilm producing, halotolerant Salinicoccus roseus: a comparative genomics-based intervention
title_full_unstemmed Delving into the lifestyle of Sundarban Wetland resident, biofilm producing, halotolerant Salinicoccus roseus: a comparative genomics-based intervention
title_short Delving into the lifestyle of Sundarban Wetland resident, biofilm producing, halotolerant Salinicoccus roseus: a comparative genomics-based intervention
title_sort delving into the lifestyle of sundarban wetland resident, biofilm producing, halotolerant salinicoccus roseus: a comparative genomics-based intervention
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10642018/
https://www.ncbi.nlm.nih.gov/pubmed/37957573
http://dx.doi.org/10.1186/s12864-023-09764-w
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