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Bacterioplankton Associated with Toxic Cyanobacteria Promote Pisum sativum (Pea) Growth and Nutritional Value through Positive Interactions

Research on Plant Growth-Promoting Bacteria (PGPB) has focused much more on rhizospheric bacteria. However, PGPB associated with toxic cyanobacterial bloom (TCB) could enter the rhizosphere through irrigation water, helping plants such as Pisum sativum L. (pea) overcome oxidative stress induced by m...

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Autores principales: Mugani, Richard, El Khalloufi, Fatima, Redouane, El Mahdi, Haida, Mohammed, Zerrifi, Soukaina El Amrani, Campos, Alexandre, Kasada, Minoru, Woodhouse, Jason, Grossart, Hans-Peter, Vasconcelos, Vitor, Oudra, Brahim
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9394358/
https://www.ncbi.nlm.nih.gov/pubmed/35893569
http://dx.doi.org/10.3390/microorganisms10081511
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author Mugani, Richard
El Khalloufi, Fatima
Redouane, El Mahdi
Haida, Mohammed
Zerrifi, Soukaina El Amrani
Campos, Alexandre
Kasada, Minoru
Woodhouse, Jason
Grossart, Hans-Peter
Vasconcelos, Vitor
Oudra, Brahim
author_facet Mugani, Richard
El Khalloufi, Fatima
Redouane, El Mahdi
Haida, Mohammed
Zerrifi, Soukaina El Amrani
Campos, Alexandre
Kasada, Minoru
Woodhouse, Jason
Grossart, Hans-Peter
Vasconcelos, Vitor
Oudra, Brahim
author_sort Mugani, Richard
collection PubMed
description Research on Plant Growth-Promoting Bacteria (PGPB) has focused much more on rhizospheric bacteria. However, PGPB associated with toxic cyanobacterial bloom (TCB) could enter the rhizosphere through irrigation water, helping plants such as Pisum sativum L. (pea) overcome oxidative stress induced by microcystin (MC) and improve plant growth and nutritional value. This study aimed to isolate bacteria associated with toxic cyanobacteria, test PGPB properties, and inoculate them as a consortium to pea seedlings irrigated with MC to investigate their role in plant protection as well as in improving growth and nutritional value. Two bacterioplankton isolates and one rhizosphere isolate were isolated and purified on a mineral salt medium supplemented with 1000 μg/L MC and identified via their 16S rRNA gene. The mixed strains were inoculated to pea seedlings in pots irrigated with 0, 50, and 100 μg/L MC. We measured the morphological and physiological parameters of pea plants at maturity and evaluated the efficiency of the plant’s enzymatic and non-enzymatic antioxidant responses to assess the role and contribution of PGPB. Both bacterioplankton isolates were identified as Starkeya sp., and the rhizobacterium was identified as Brevundimonas aurantiaca. MC addition significantly (p < 0.05) reduced all the growth parameters of the pea, i.e., total chlorophyll content, leaf quantum yield, stomatal conductance, carotenoids, and polyphenol contents, in an MC concentration-dependent manner, while bacterial presence positively affected all the measured parameters. In the MC treatment, the levels of the pea’s antioxidant traits, including SOD, CAT, POD, PPO, GST, and ascorbic acid, were increased in the sterile pots. In contrast, these levels were reduced with double and triple PGPB addition. Additionally, nutritional values such as sugars, proteins, and minerals (Ca and K) in pea fruits were reduced under MC exposure but increased with PGPB addition. Overall, in the presence of MC, PGPB seem to positively interact with pea plants and thus may constitute a natural alternative for soil fertilization when irrigated with cyanotoxin-contaminated water, increasing the yield and nutritional value of crops.
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spelling pubmed-93943582022-08-23 Bacterioplankton Associated with Toxic Cyanobacteria Promote Pisum sativum (Pea) Growth and Nutritional Value through Positive Interactions Mugani, Richard El Khalloufi, Fatima Redouane, El Mahdi Haida, Mohammed Zerrifi, Soukaina El Amrani Campos, Alexandre Kasada, Minoru Woodhouse, Jason Grossart, Hans-Peter Vasconcelos, Vitor Oudra, Brahim Microorganisms Article Research on Plant Growth-Promoting Bacteria (PGPB) has focused much more on rhizospheric bacteria. However, PGPB associated with toxic cyanobacterial bloom (TCB) could enter the rhizosphere through irrigation water, helping plants such as Pisum sativum L. (pea) overcome oxidative stress induced by microcystin (MC) and improve plant growth and nutritional value. This study aimed to isolate bacteria associated with toxic cyanobacteria, test PGPB properties, and inoculate them as a consortium to pea seedlings irrigated with MC to investigate their role in plant protection as well as in improving growth and nutritional value. Two bacterioplankton isolates and one rhizosphere isolate were isolated and purified on a mineral salt medium supplemented with 1000 μg/L MC and identified via their 16S rRNA gene. The mixed strains were inoculated to pea seedlings in pots irrigated with 0, 50, and 100 μg/L MC. We measured the morphological and physiological parameters of pea plants at maturity and evaluated the efficiency of the plant’s enzymatic and non-enzymatic antioxidant responses to assess the role and contribution of PGPB. Both bacterioplankton isolates were identified as Starkeya sp., and the rhizobacterium was identified as Brevundimonas aurantiaca. MC addition significantly (p < 0.05) reduced all the growth parameters of the pea, i.e., total chlorophyll content, leaf quantum yield, stomatal conductance, carotenoids, and polyphenol contents, in an MC concentration-dependent manner, while bacterial presence positively affected all the measured parameters. In the MC treatment, the levels of the pea’s antioxidant traits, including SOD, CAT, POD, PPO, GST, and ascorbic acid, were increased in the sterile pots. In contrast, these levels were reduced with double and triple PGPB addition. Additionally, nutritional values such as sugars, proteins, and minerals (Ca and K) in pea fruits were reduced under MC exposure but increased with PGPB addition. Overall, in the presence of MC, PGPB seem to positively interact with pea plants and thus may constitute a natural alternative for soil fertilization when irrigated with cyanotoxin-contaminated water, increasing the yield and nutritional value of crops. MDPI 2022-07-26 /pmc/articles/PMC9394358/ /pubmed/35893569 http://dx.doi.org/10.3390/microorganisms10081511 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Mugani, Richard
El Khalloufi, Fatima
Redouane, El Mahdi
Haida, Mohammed
Zerrifi, Soukaina El Amrani
Campos, Alexandre
Kasada, Minoru
Woodhouse, Jason
Grossart, Hans-Peter
Vasconcelos, Vitor
Oudra, Brahim
Bacterioplankton Associated with Toxic Cyanobacteria Promote Pisum sativum (Pea) Growth and Nutritional Value through Positive Interactions
title Bacterioplankton Associated with Toxic Cyanobacteria Promote Pisum sativum (Pea) Growth and Nutritional Value through Positive Interactions
title_full Bacterioplankton Associated with Toxic Cyanobacteria Promote Pisum sativum (Pea) Growth and Nutritional Value through Positive Interactions
title_fullStr Bacterioplankton Associated with Toxic Cyanobacteria Promote Pisum sativum (Pea) Growth and Nutritional Value through Positive Interactions
title_full_unstemmed Bacterioplankton Associated with Toxic Cyanobacteria Promote Pisum sativum (Pea) Growth and Nutritional Value through Positive Interactions
title_short Bacterioplankton Associated with Toxic Cyanobacteria Promote Pisum sativum (Pea) Growth and Nutritional Value through Positive Interactions
title_sort bacterioplankton associated with toxic cyanobacteria promote pisum sativum (pea) growth and nutritional value through positive interactions
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9394358/
https://www.ncbi.nlm.nih.gov/pubmed/35893569
http://dx.doi.org/10.3390/microorganisms10081511
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