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The Dual Role of the Glycolipid Envelope in Different Cell Types of the Multicellular Cyanobacterium Anabaena variabilis ATCC 29413

Anabaena variabilis is a filamentous cyanobacterium that is capable to differentiate specialized cells, the heterocysts and akinetes, to survive under different stress conditions. Under nitrogen limited condition, heterocysts provide the filament with nitrogen by fixing N(2). Akinetes are spore-like...

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Autores principales: Garg, Ritu, Maldener, Iris
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8064123/
https://www.ncbi.nlm.nih.gov/pubmed/33897656
http://dx.doi.org/10.3389/fmicb.2021.645028
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author Garg, Ritu
Maldener, Iris
author_facet Garg, Ritu
Maldener, Iris
author_sort Garg, Ritu
collection PubMed
description Anabaena variabilis is a filamentous cyanobacterium that is capable to differentiate specialized cells, the heterocysts and akinetes, to survive under different stress conditions. Under nitrogen limited condition, heterocysts provide the filament with nitrogen by fixing N(2). Akinetes are spore-like dormant cells that allow survival during adverse environmental conditions. Both cell types are characterized by the presence of a thick multilayered envelope, including a glycolipid layer. While in the heterocyst this glycolipid layer is required for the maintenance of a microoxic environment and nitrogen fixation, its function in akinetes is completely unknown. Therefore, we constructed a mutant deficient in glycolipid synthesis and investigated the performance of heterocysts and akinetes in that mutant strain. We chose to delete the gene Ava_2595, which is homolog to the known hglB gene, encoding a putative polyketide synthase previously shown to be involved in heterocyst glycolipid synthesis in Anabaena sp. PCC 7120, a species which does not form akinetes. Under the respective conditions, the Ava_2595 null mutant strain formed aberrant heterocysts and akinete-like cells, in which the specific glycolipid layers were absent. This confirmed firstly that both cell types use a glycolipid of identical chemical composition in their special envelopes and, secondly, that HglB is essential for glycolipid synthesis in both types of differentiated cells. As a consequence, the mutant was not able to fix N(2) and to grow under diazotrophic conditions. Furthermore, the akinetes lacking the glycolipids showed a severely reduced tolerance to stress conditions, but could germinate normally under standard conditions. This demonstrates the importance of the glycolipid layer for the ability of akinetes as spore-like dormant cells to withstand freezing, desiccation, oxidative stress and attack by lytic enzymes. Our study established the dual role of the glycolipid layer in fulfilling different functions in the evolutionary-related specialized cells of cyanobacteria. It also indicates the existence of a common pathway involving HglB for the synthesis of glycolipids in heterocysts and akinetes.
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spelling pubmed-80641232021-04-24 The Dual Role of the Glycolipid Envelope in Different Cell Types of the Multicellular Cyanobacterium Anabaena variabilis ATCC 29413 Garg, Ritu Maldener, Iris Front Microbiol Microbiology Anabaena variabilis is a filamentous cyanobacterium that is capable to differentiate specialized cells, the heterocysts and akinetes, to survive under different stress conditions. Under nitrogen limited condition, heterocysts provide the filament with nitrogen by fixing N(2). Akinetes are spore-like dormant cells that allow survival during adverse environmental conditions. Both cell types are characterized by the presence of a thick multilayered envelope, including a glycolipid layer. While in the heterocyst this glycolipid layer is required for the maintenance of a microoxic environment and nitrogen fixation, its function in akinetes is completely unknown. Therefore, we constructed a mutant deficient in glycolipid synthesis and investigated the performance of heterocysts and akinetes in that mutant strain. We chose to delete the gene Ava_2595, which is homolog to the known hglB gene, encoding a putative polyketide synthase previously shown to be involved in heterocyst glycolipid synthesis in Anabaena sp. PCC 7120, a species which does not form akinetes. Under the respective conditions, the Ava_2595 null mutant strain formed aberrant heterocysts and akinete-like cells, in which the specific glycolipid layers were absent. This confirmed firstly that both cell types use a glycolipid of identical chemical composition in their special envelopes and, secondly, that HglB is essential for glycolipid synthesis in both types of differentiated cells. As a consequence, the mutant was not able to fix N(2) and to grow under diazotrophic conditions. Furthermore, the akinetes lacking the glycolipids showed a severely reduced tolerance to stress conditions, but could germinate normally under standard conditions. This demonstrates the importance of the glycolipid layer for the ability of akinetes as spore-like dormant cells to withstand freezing, desiccation, oxidative stress and attack by lytic enzymes. Our study established the dual role of the glycolipid layer in fulfilling different functions in the evolutionary-related specialized cells of cyanobacteria. It also indicates the existence of a common pathway involving HglB for the synthesis of glycolipids in heterocysts and akinetes. Frontiers Media S.A. 2021-04-09 /pmc/articles/PMC8064123/ /pubmed/33897656 http://dx.doi.org/10.3389/fmicb.2021.645028 Text en Copyright © 2021 Garg and Maldener. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Garg, Ritu
Maldener, Iris
The Dual Role of the Glycolipid Envelope in Different Cell Types of the Multicellular Cyanobacterium Anabaena variabilis ATCC 29413
title The Dual Role of the Glycolipid Envelope in Different Cell Types of the Multicellular Cyanobacterium Anabaena variabilis ATCC 29413
title_full The Dual Role of the Glycolipid Envelope in Different Cell Types of the Multicellular Cyanobacterium Anabaena variabilis ATCC 29413
title_fullStr The Dual Role of the Glycolipid Envelope in Different Cell Types of the Multicellular Cyanobacterium Anabaena variabilis ATCC 29413
title_full_unstemmed The Dual Role of the Glycolipid Envelope in Different Cell Types of the Multicellular Cyanobacterium Anabaena variabilis ATCC 29413
title_short The Dual Role of the Glycolipid Envelope in Different Cell Types of the Multicellular Cyanobacterium Anabaena variabilis ATCC 29413
title_sort dual role of the glycolipid envelope in different cell types of the multicellular cyanobacterium anabaena variabilis atcc 29413
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8064123/
https://www.ncbi.nlm.nih.gov/pubmed/33897656
http://dx.doi.org/10.3389/fmicb.2021.645028
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