Microbial degradation of pyridine: a proposed nitrogen metabolism pathway deciphered in marine mangrove Bacillus aryabhattai strain NM1-A2

Abstract Background Diverse microbes, such as bacteria, are of immense worth to mangrove ecosystems due to their adaptability to salinity and variable environmental characteristics conditions. Pyridine and its derivatives compose most heterocyclic aromatic compounds largely produced by human activit...

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Main Authors: Muhammad Kashif, Lirong Bai, Jianwen Xiong, Shuming Mo, Yimeng Sang, Kunmei Huang, Jingjing Song, Syed Jalil Shah, Sohail Khan, Taj Malook Khan, Chengjian Jiang
Format: Article
Language:English
Published: SpringerOpen 2023-12-01
Series:Chemical and Biological Technologies in Agriculture
Subjects:
Online Access:https://doi.org/10.1186/s40538-023-00513-5
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author Muhammad Kashif
Lirong Bai
Jianwen Xiong
Shuming Mo
Yimeng Sang
Kunmei Huang
Jingjing Song
Syed Jalil Shah
Sohail Khan
Taj Malook Khan
Chengjian Jiang
author_facet Muhammad Kashif
Lirong Bai
Jianwen Xiong
Shuming Mo
Yimeng Sang
Kunmei Huang
Jingjing Song
Syed Jalil Shah
Sohail Khan
Taj Malook Khan
Chengjian Jiang
author_sort Muhammad Kashif
collection DOAJ
description Abstract Background Diverse microbes, such as bacteria, are of immense worth to mangrove ecosystems due to their adaptability to salinity and variable environmental characteristics conditions. Pyridine and its derivatives compose most heterocyclic aromatic compounds largely produced by human activities that lead to environmental pollution. Bacteria have a crucial role in the nutrient cycling of carbon and nitrogen etc., to understand their functional involvement with environmental factors or ecosystem functioning as well as the species invasion and domestic or agriculture pyridine degradation pollution activities that threaten the mangrove ecosystem. Methods This work established the genetic-based molecular degradation of organic compounds in the mangrove ecosystem, which ultimately makes the availability of nutrients. As well as the effects of various abiotic factors on pyridine degradation to discover the pyridine degradation and the removal of ammonia nitrogen and the proposed nitrogen metabolism pathway. Results The novel bacterial strain NM1-A2 was isolated from mangrove sediments and, after 16S rRNA gene sequence analysis identified as Bacillus aryabhattai. NM1-A2 completely degraded pyridine within a 100 h incubation period at a temperature of 35 °C, an initial pH of 7.0, glucose and a pyridine concentration of 500 mg/L. The pseudo-first-order kinetics model described the pyridine biodegradation profile of NM1-A2 well. Interestingly, within 96 h the strain achieved almost complete pyridine degradation with a total organic carbon (TOC) removal of 87.9% ± 0.19% (from 377.52 ± 6.9 mg/L to 45.65 ± 0.14 mg/L). Within 96 h, the pyridine ring in the total nitrogen (TN) fraction at the maximum concentration of 55.31 ± 0.17 mg/L, furtherly 51.3% ± 2.39% of (TN) converted into Ammonia nitrogen (NH4 +-N). Furthermore, NM1-A2 exhibited its pyridine biodegradation activity decreased by only 4% after three consecutive cycles (48 h each). Moreover, NM1-A2 possessed nrt-ABCD nitrate transport family and gltABCD operons that participate in the activities of glutamine and glutamate synthetase in NH4 + conversion in the nitrogen cycle. Furthermore, the nitrogen metabolism genes (nrtA, nrtB, nrtC, nirB, nirD, gltB, gltD, glnA) exhibited expression in NM1-A2. Conclusion This research offers a potential treatment strategy for pyridine degradation in the mangrove ecosystem. Graphical Abstract
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spelling doaj.art-1c42c67339eb4964845746681b34dc922023-12-17T12:09:14ZengSpringerOpenChemical and Biological Technologies in Agriculture2196-56412023-12-0110111210.1186/s40538-023-00513-5Microbial degradation of pyridine: a proposed nitrogen metabolism pathway deciphered in marine mangrove Bacillus aryabhattai strain NM1-A2Muhammad Kashif0Lirong Bai1Jianwen Xiong2Shuming Mo3Yimeng Sang4Kunmei Huang5Jingjing Song6Syed Jalil Shah7Sohail Khan8Taj Malook Khan9Chengjian Jiang10National Engineering Research Center for Non-Food Biorefinery, State Key Laboratory of Non-Food Biomass and Enzyme Technology, Guangxi Research Center for Biological Science and Technology, Guangxi Academy of SciencesGuangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, Beibu Gulf UniversityLiuzhou Key Laboratory of Plant-Derived Ingredients of Liuzhou Luosifen, Liuzhou Special Food Flavor and Quality Control Research Center of Engineering Technology, Department of Food and Chemical Engineering, Liuzhou Institute of TechnologyNational Engineering Research Center for Non-Food Biorefinery, State Key Laboratory of Non-Food Biomass and Enzyme Technology, Guangxi Research Center for Biological Science and Technology, Guangxi Academy of SciencesState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Research Center for Microbial and Enzyme Engineering Technology, College of Life Science and Technology, Guangxi UniversityState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Research Center for Microbial and Enzyme Engineering Technology, College of Life Science and Technology, Guangxi UniversityGuangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, Beibu Gulf UniversityMOE Key Laboratory of New Processing Technology for Non-Ferrous Metals and Materials, Guangxi Key Laboratory of Processing for Non-Ferrous Metals and Featured Materials, School of Chemistry and Chemical Engineering, Guangxi UniversityCollege of Resources and Environment, University of Chinese Academy of SciencesResearch Center for Drug Discovery and Functional Food, Southwest Medical UniversityNational Engineering Research Center for Non-Food Biorefinery, State Key Laboratory of Non-Food Biomass and Enzyme Technology, Guangxi Research Center for Biological Science and Technology, Guangxi Academy of SciencesAbstract Background Diverse microbes, such as bacteria, are of immense worth to mangrove ecosystems due to their adaptability to salinity and variable environmental characteristics conditions. Pyridine and its derivatives compose most heterocyclic aromatic compounds largely produced by human activities that lead to environmental pollution. Bacteria have a crucial role in the nutrient cycling of carbon and nitrogen etc., to understand their functional involvement with environmental factors or ecosystem functioning as well as the species invasion and domestic or agriculture pyridine degradation pollution activities that threaten the mangrove ecosystem. Methods This work established the genetic-based molecular degradation of organic compounds in the mangrove ecosystem, which ultimately makes the availability of nutrients. As well as the effects of various abiotic factors on pyridine degradation to discover the pyridine degradation and the removal of ammonia nitrogen and the proposed nitrogen metabolism pathway. Results The novel bacterial strain NM1-A2 was isolated from mangrove sediments and, after 16S rRNA gene sequence analysis identified as Bacillus aryabhattai. NM1-A2 completely degraded pyridine within a 100 h incubation period at a temperature of 35 °C, an initial pH of 7.0, glucose and a pyridine concentration of 500 mg/L. The pseudo-first-order kinetics model described the pyridine biodegradation profile of NM1-A2 well. Interestingly, within 96 h the strain achieved almost complete pyridine degradation with a total organic carbon (TOC) removal of 87.9% ± 0.19% (from 377.52 ± 6.9 mg/L to 45.65 ± 0.14 mg/L). Within 96 h, the pyridine ring in the total nitrogen (TN) fraction at the maximum concentration of 55.31 ± 0.17 mg/L, furtherly 51.3% ± 2.39% of (TN) converted into Ammonia nitrogen (NH4 +-N). Furthermore, NM1-A2 exhibited its pyridine biodegradation activity decreased by only 4% after three consecutive cycles (48 h each). Moreover, NM1-A2 possessed nrt-ABCD nitrate transport family and gltABCD operons that participate in the activities of glutamine and glutamate synthetase in NH4 + conversion in the nitrogen cycle. Furthermore, the nitrogen metabolism genes (nrtA, nrtB, nrtC, nirB, nirD, gltB, gltD, glnA) exhibited expression in NM1-A2. Conclusion This research offers a potential treatment strategy for pyridine degradation in the mangrove ecosystem. Graphical Abstracthttps://doi.org/10.1186/s40538-023-00513-5Bacillus aryabhattaiPyridine degradationNitrogen metabolismMangrove environment
spellingShingle Muhammad Kashif
Lirong Bai
Jianwen Xiong
Shuming Mo
Yimeng Sang
Kunmei Huang
Jingjing Song
Syed Jalil Shah
Sohail Khan
Taj Malook Khan
Chengjian Jiang
Microbial degradation of pyridine: a proposed nitrogen metabolism pathway deciphered in marine mangrove Bacillus aryabhattai strain NM1-A2
Chemical and Biological Technologies in Agriculture
Bacillus aryabhattai
Pyridine degradation
Nitrogen metabolism
Mangrove environment
title Microbial degradation of pyridine: a proposed nitrogen metabolism pathway deciphered in marine mangrove Bacillus aryabhattai strain NM1-A2
title_full Microbial degradation of pyridine: a proposed nitrogen metabolism pathway deciphered in marine mangrove Bacillus aryabhattai strain NM1-A2
title_fullStr Microbial degradation of pyridine: a proposed nitrogen metabolism pathway deciphered in marine mangrove Bacillus aryabhattai strain NM1-A2
title_full_unstemmed Microbial degradation of pyridine: a proposed nitrogen metabolism pathway deciphered in marine mangrove Bacillus aryabhattai strain NM1-A2
title_short Microbial degradation of pyridine: a proposed nitrogen metabolism pathway deciphered in marine mangrove Bacillus aryabhattai strain NM1-A2
title_sort microbial degradation of pyridine a proposed nitrogen metabolism pathway deciphered in marine mangrove bacillus aryabhattai strain nm1 a2
topic Bacillus aryabhattai
Pyridine degradation
Nitrogen metabolism
Mangrove environment
url https://doi.org/10.1186/s40538-023-00513-5
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