Homospermidine biosynthesis in the cyanobacterium Anabaena requires a deoxyhypusine synthase homologue and is essential for normal diazotrophic growth

Polyamines are primordial, small organic polycations present in almost all cells, but their roles in bacteria are poorly understood. sym‐Homospermidine is the dominant polyamine in the filamentous, N2‐fixing, heterocyst‐forming cyanobacterium Anabaena sp. PCC 7120. Synthesis of homospermidine was dependent on speA (encoding arginine decarboxylase), speB (agmatinase) and speY (deoxyhypusine synthase homologue), which in bacteria is an unprecedented pathway. Inactivation of any of these genes impaired diazotrophic growth. Heterocyst differentiation in the speA mutant was blocked at an early step, after induction of the regulatory gene hetR but before production of heterocyst‐specific glycolipids (HGL). In contrast, the speY mutant produced HGL and showed slow diazotrophic growth. Analysis of fusions to green fluorescent protein revealed that SpeA (like SpeB previously described) accumulates at higher levels in vegetative cells than in heterocysts, and that SpeY accumulates in vegetative cells but also at significant levels in heterocysts. The homospermidine biosynthetic pathway is therefore active primarily in vegetative cells but the last step can be completed in heterocysts. Our findings indicate an important role for polyamines in the diazotrophic biology of Anabaena. Furthermore, inactivation of a gene cluster (potADB) encoding a polyamine ABC transporter disrupted diazotrophic growth, corroborating the importance of polyamine homeostasis in Anabaena.

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Bibliographic Details
Main Authors: Burnat, Mireia, Li, Bin, Kim, Sok-Ho, Michael, Anthony J., Flores, Enrique
Other Authors: European Commission
Format: artículo biblioteca
Published: Blackwell Publishing 2018-09
Subjects:Heterocyst differentiation, Homospermidine biosynthesis, Nitrogen fixation, Polyamines., Cyanobacteria,
Online Access:http://hdl.handle.net/10261/173217
http://dx.doi.org/10.13039/501100003329
http://dx.doi.org/10.13039/100007914
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/501100011033
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spelling dig-icm-es-10261-1732172020-12-13T08:45:38Z Homospermidine biosynthesis in the cyanobacterium Anabaena requires a deoxyhypusine synthase homologue and is essential for normal diazotrophic growth Burnat, Mireia Li, Bin Kim, Sok-Ho Michael, Anthony J. Flores, Enrique European Commission Agencia Estatal de Investigación (España) Ministerio de Economía y Competitividad (España) Ministerio de Ciencia, Innovación y Universidades (España) University of Texas Southwestern Medical Center Heterocyst differentiation Homospermidine biosynthesis Nitrogen fixation Polyamines. Cyanobacteria Polyamines are primordial, small organic polycations present in almost all cells, but their roles in bacteria are poorly understood. sym‐Homospermidine is the dominant polyamine in the filamentous, N2‐fixing, heterocyst‐forming cyanobacterium Anabaena sp. PCC 7120. Synthesis of homospermidine was dependent on speA (encoding arginine decarboxylase), speB (agmatinase) and speY (deoxyhypusine synthase homologue), which in bacteria is an unprecedented pathway. Inactivation of any of these genes impaired diazotrophic growth. Heterocyst differentiation in the speA mutant was blocked at an early step, after induction of the regulatory gene hetR but before production of heterocyst‐specific glycolipids (HGL). In contrast, the speY mutant produced HGL and showed slow diazotrophic growth. Analysis of fusions to green fluorescent protein revealed that SpeA (like SpeB previously described) accumulates at higher levels in vegetative cells than in heterocysts, and that SpeY accumulates in vegetative cells but also at significant levels in heterocysts. The homospermidine biosynthetic pathway is therefore active primarily in vegetative cells but the last step can be completed in heterocysts. Our findings indicate an important role for polyamines in the diazotrophic biology of Anabaena. Furthermore, inactivation of a gene cluster (potADB) encoding a polyamine ABC transporter disrupted diazotrophic growth, corroborating the importance of polyamine homeostasis in Anabaena. Work was supported by grants number BFU2014‐56757‐P and BFU2017‐88202‐P from Agencia Estatal de Investigación, Spain, co‐financed by the European Regional Development Grant (EF) and by a seed grant from UT Southwestern Medical Center (AJM). Peer Reviewed 2018-12-14T09:17:19Z 2018-12-14T09:17:19Z 2018-09 2018-12-14T09:17:19Z artículo http://purl.org/coar/resource_type/c_6501 doi: 10.1111/mmi.14006 issn: 0950-382X Molecular Microbiology 109(6): 763-780 (2018) http://hdl.handle.net/10261/173217 10.1111/mmi.14006 http://dx.doi.org/10.13039/501100003329 http://dx.doi.org/10.13039/100007914 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100011033 #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# BFU2017‐88202‐P/AEI/10.13039/501100011033 info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BFU2014‐56757‐P info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/BFU2017‐88202‐P Postprint http://doi.org/10.1111/mmi.14006 Sí open Blackwell Publishing
institution ICM ES
collection DSpace
country España
countrycode ES
component Bibliográfico
access En linea
databasecode dig-icm-es
tag biblioteca
region Europa del Sur
libraryname Biblioteca del ICM España
topic Heterocyst differentiation
Homospermidine biosynthesis
Nitrogen fixation
Polyamines.
Cyanobacteria
Heterocyst differentiation
Homospermidine biosynthesis
Nitrogen fixation
Polyamines.
Cyanobacteria
spellingShingle Heterocyst differentiation
Homospermidine biosynthesis
Nitrogen fixation
Polyamines.
Cyanobacteria
Heterocyst differentiation
Homospermidine biosynthesis
Nitrogen fixation
Polyamines.
Cyanobacteria
Burnat, Mireia
Li, Bin
Kim, Sok-Ho
Michael, Anthony J.
Flores, Enrique
Homospermidine biosynthesis in the cyanobacterium Anabaena requires a deoxyhypusine synthase homologue and is essential for normal diazotrophic growth
description Polyamines are primordial, small organic polycations present in almost all cells, but their roles in bacteria are poorly understood. sym‐Homospermidine is the dominant polyamine in the filamentous, N2‐fixing, heterocyst‐forming cyanobacterium Anabaena sp. PCC 7120. Synthesis of homospermidine was dependent on speA (encoding arginine decarboxylase), speB (agmatinase) and speY (deoxyhypusine synthase homologue), which in bacteria is an unprecedented pathway. Inactivation of any of these genes impaired diazotrophic growth. Heterocyst differentiation in the speA mutant was blocked at an early step, after induction of the regulatory gene hetR but before production of heterocyst‐specific glycolipids (HGL). In contrast, the speY mutant produced HGL and showed slow diazotrophic growth. Analysis of fusions to green fluorescent protein revealed that SpeA (like SpeB previously described) accumulates at higher levels in vegetative cells than in heterocysts, and that SpeY accumulates in vegetative cells but also at significant levels in heterocysts. The homospermidine biosynthetic pathway is therefore active primarily in vegetative cells but the last step can be completed in heterocysts. Our findings indicate an important role for polyamines in the diazotrophic biology of Anabaena. Furthermore, inactivation of a gene cluster (potADB) encoding a polyamine ABC transporter disrupted diazotrophic growth, corroborating the importance of polyamine homeostasis in Anabaena.
author2 European Commission
author_facet European Commission
Burnat, Mireia
Li, Bin
Kim, Sok-Ho
Michael, Anthony J.
Flores, Enrique
format artículo
topic_facet Heterocyst differentiation
Homospermidine biosynthesis
Nitrogen fixation
Polyamines.
Cyanobacteria
author Burnat, Mireia
Li, Bin
Kim, Sok-Ho
Michael, Anthony J.
Flores, Enrique
author_sort Burnat, Mireia
title Homospermidine biosynthesis in the cyanobacterium Anabaena requires a deoxyhypusine synthase homologue and is essential for normal diazotrophic growth
title_short Homospermidine biosynthesis in the cyanobacterium Anabaena requires a deoxyhypusine synthase homologue and is essential for normal diazotrophic growth
title_full Homospermidine biosynthesis in the cyanobacterium Anabaena requires a deoxyhypusine synthase homologue and is essential for normal diazotrophic growth
title_fullStr Homospermidine biosynthesis in the cyanobacterium Anabaena requires a deoxyhypusine synthase homologue and is essential for normal diazotrophic growth
title_full_unstemmed Homospermidine biosynthesis in the cyanobacterium Anabaena requires a deoxyhypusine synthase homologue and is essential for normal diazotrophic growth
title_sort homospermidine biosynthesis in the cyanobacterium anabaena requires a deoxyhypusine synthase homologue and is essential for normal diazotrophic growth
publisher Blackwell Publishing
publishDate 2018-09
url http://hdl.handle.net/10261/173217
http://dx.doi.org/10.13039/501100003329
http://dx.doi.org/10.13039/100007914
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/501100011033
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