Unresolved mystery of cyclic nucleotide second messengers, periplasmic acid phosphatases and bacterial natural competence

We recently characterized the competitive inhibition of cyclic AMP (cAMP) on three periplasmic acid phosphatases, AphAHi, NadNHi, and eP4 (HelHi), in Haemophilus influenzae Rd KW20. This inhibitory effect is vital for orchestrating the nutritional growth and competence development in KW20. Initially...

Full description

Saved in:
Bibliographic Details
Main Authors: Kristina Kronborg, Yong Everett Zhang
Format: Article
Language:English
Published: Shared Science Publishers OG 2024-07-01
Series:Microbial Cell
Subjects:
Online Access:http://microbialcell.com/researcharticles/2024a-kronborg-microbial-cell/
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850228271925428224
author Kristina Kronborg
Yong Everett Zhang
author_facet Kristina Kronborg
Yong Everett Zhang
author_sort Kristina Kronborg
collection DOAJ
description We recently characterized the competitive inhibition of cyclic AMP (cAMP) on three periplasmic acid phosphatases, AphAHi, NadNHi, and eP4 (HelHi), in Haemophilus influenzae Rd KW20. This inhibitory effect is vital for orchestrating the nutritional growth and competence development in KW20. Initially discovered in Escherichia coli, the function of AphA remains however obscure. This study investigates the regulation of E. coli aphA expression under nutrient starvation conditions. Using transcriptional reporters with truncated aphA promoter sequences, we found that starvations of carbon and phosphate, but not amino acid, stimulated aphA expression through distinct promoter regions. Deletions of crp or cyaA abolished aphA expression, confirming their crucial roles. Conversely, CytR deletion increased aphA expression, suggesting CytR's role as a repressor of aphA expression. Additionally, we extended the study of three other second messengers, i.e., cyclic GMP, cyclic UMP, and cyclic CMP, each sharing structural similarities with cAMP. Notably, cGMP competitively inhibits AphAHi's acid phosphatase activity akin to cAMP. In contrast, both cUMP and cCMP stimulate AphAHi's phosphatase activity in a concentration dependent manner. Collectively, these data imply a complicated connection between nucleotide metabolism, AphA, cyclic purine and pyrimidine nucleotides in bacterial nutrient uptake and natural competence.
format Article
id doaj-art-8d16de019b4a4cda9a1fec7b28b2ed92
institution OA Journals
issn 2311-2638
language English
publishDate 2024-07-01
publisher Shared Science Publishers OG
record_format Article
series Microbial Cell
spelling doaj-art-8d16de019b4a4cda9a1fec7b28b2ed922025-08-20T02:04:34ZengShared Science Publishers OGMicrobial Cell2311-26382024-07-011123524110.15698/mic2024.07.828Unresolved mystery of cyclic nucleotide second messengers, periplasmic acid phosphatases and bacterial natural competenceKristina Kronborg0Yong Everett Zhang1Department of Biology, University of Copenhagen, Copenhagen, DK­2200, DenmarkDepartment of Biology, University of Copenhagen, Copenhagen, DK­2200, DenmarkWe recently characterized the competitive inhibition of cyclic AMP (cAMP) on three periplasmic acid phosphatases, AphAHi, NadNHi, and eP4 (HelHi), in Haemophilus influenzae Rd KW20. This inhibitory effect is vital for orchestrating the nutritional growth and competence development in KW20. Initially discovered in Escherichia coli, the function of AphA remains however obscure. This study investigates the regulation of E. coli aphA expression under nutrient starvation conditions. Using transcriptional reporters with truncated aphA promoter sequences, we found that starvations of carbon and phosphate, but not amino acid, stimulated aphA expression through distinct promoter regions. Deletions of crp or cyaA abolished aphA expression, confirming their crucial roles. Conversely, CytR deletion increased aphA expression, suggesting CytR's role as a repressor of aphA expression. Additionally, we extended the study of three other second messengers, i.e., cyclic GMP, cyclic UMP, and cyclic CMP, each sharing structural similarities with cAMP. Notably, cGMP competitively inhibits AphAHi's acid phosphatase activity akin to cAMP. In contrast, both cUMP and cCMP stimulate AphAHi's phosphatase activity in a concentration dependent manner. Collectively, these data imply a complicated connection between nucleotide metabolism, AphA, cyclic purine and pyrimidine nucleotides in bacterial nutrient uptake and natural competence.http://microbialcell.com/researcharticles/2024a-kronborg-microbial-cell/campcgmpccmpcumpnatural competencehaemophilus influenzae
spellingShingle Kristina Kronborg
Yong Everett Zhang
Unresolved mystery of cyclic nucleotide second messengers, periplasmic acid phosphatases and bacterial natural competence
Microbial Cell
camp
cgmp
ccmp
cump
natural competence
haemophilus influenzae
title Unresolved mystery of cyclic nucleotide second messengers, periplasmic acid phosphatases and bacterial natural competence
title_full Unresolved mystery of cyclic nucleotide second messengers, periplasmic acid phosphatases and bacterial natural competence
title_fullStr Unresolved mystery of cyclic nucleotide second messengers, periplasmic acid phosphatases and bacterial natural competence
title_full_unstemmed Unresolved mystery of cyclic nucleotide second messengers, periplasmic acid phosphatases and bacterial natural competence
title_short Unresolved mystery of cyclic nucleotide second messengers, periplasmic acid phosphatases and bacterial natural competence
title_sort unresolved mystery of cyclic nucleotide second messengers periplasmic acid phosphatases and bacterial natural competence
topic camp
cgmp
ccmp
cump
natural competence
haemophilus influenzae
url http://microbialcell.com/researcharticles/2024a-kronborg-microbial-cell/
work_keys_str_mv AT kristinakronborg unresolvedmysteryofcyclicnucleotidesecondmessengersperiplasmicacidphosphatasesandbacterialnaturalcompetence
AT yongeverettzhang unresolvedmysteryofcyclicnucleotidesecondmessengersperiplasmicacidphosphatasesandbacterialnaturalcompetence