Attenuation of the Type IV Pilus Retraction Motor Influences <named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Social and Infection Behavior

ABSTRACT Retraction of the type IV pilus (Tfp) mediates DNA uptake, motility, and social and infection behavior in a wide variety of prokaryotes. To date, investigations into Tfp retraction-dependent activities have used a mutant deleted of PilT, the ATPase motor protein that causes the pilus fiber...

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Autores principales:	Alyson M. Hockenberry, Danielle M. Hutchens, Al Agellon, Magdalene So
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e5ea5d8d9b66451d8a8311baf10459a3
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spelling	oai:doaj.org-article:e5ea5d8d9b66451d8a8311baf10459a32021-11-15T15:50:15ZAttenuation of the Type IV Pilus Retraction Motor Influences <named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Social and Infection Behavior10.1128/mBio.01994-162150-7511https://doaj.org/article/e5ea5d8d9b66451d8a8311baf10459a32016-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01994-16https://doaj.org/toc/2150-7511ABSTRACT Retraction of the type IV pilus (Tfp) mediates DNA uptake, motility, and social and infection behavior in a wide variety of prokaryotes. To date, investigations into Tfp retraction-dependent activities have used a mutant deleted of PilT, the ATPase motor protein that causes the pilus fiber to retract. ΔpilT cells are nontransformable, nonmotile, and cannot aggregate into microcolonies. We tested the hypothesis that these retraction-dependent activities are sensitive to the strength of PilT enzymatic activity by using the pathogen Neisseria gonorrhoeae as a model. We constructed an N. gonorrhoeae mutant with an amino acid substitution in the PilT Walker B box (a substitution of cysteine for leucine at position 201, encoded by pilTL201C). Purified PilTL201C forms a native hexamer, but mutant hexamers hydrolyze ATP at half the maximal rate. N. gonorrhoeae pilTL201C cells produce Tfp fibers, crawl at the same speed as the wild-type (wt) parent, and are equally transformable. However, the social behavior of pilTL201C cells is intermediate between the behaviors of wt and ΔpilT cells. The infection behavior of pilTL201C is also defective, due to its failure to activate the epidermal growth factor receptor (EGFR)-heparin-binding EGF-like growth factor (HB-EGF) pathway. Our study indicates that pilus retraction, per se, is not sufficient for N. gonorrhoeae microcolony formation or infectivity; rather, these activities are sensitive to the strength of PilT enzymatic activity. We discuss the implications of these findings for Neisseria pathogenesis in the context of mechanobiology. IMPORTANCE Type IV pili are fibers expressed on the surface of many bacteria. Neisseria gonorrhoeae cells crawl, take up DNA, and communicate with each other and with human cells by retracting these fibers. Here, we show that an N. gonorrhoeae mutant expressing an enzymatically weakened type IV pilus retraction motor still crawls and takes up DNA normally. However, mutant cells exhibit abnormal social behavior, and they are less infective because they fail to activate the epidermal growth factor receptor. Our study shows that N. gonorrhoeae social and infection behaviors are sensitive to the strength of the retraction motor enzyme.Alyson M. HockenberryDanielle M. HutchensAl AgellonMagdalene SoAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 6 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Alyson M. Hockenberry Danielle M. Hutchens Al Agellon Magdalene So Attenuation of the Type IV Pilus Retraction Motor Influences <named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Social and Infection Behavior
description	ABSTRACT Retraction of the type IV pilus (Tfp) mediates DNA uptake, motility, and social and infection behavior in a wide variety of prokaryotes. To date, investigations into Tfp retraction-dependent activities have used a mutant deleted of PilT, the ATPase motor protein that causes the pilus fiber to retract. ΔpilT cells are nontransformable, nonmotile, and cannot aggregate into microcolonies. We tested the hypothesis that these retraction-dependent activities are sensitive to the strength of PilT enzymatic activity by using the pathogen Neisseria gonorrhoeae as a model. We constructed an N. gonorrhoeae mutant with an amino acid substitution in the PilT Walker B box (a substitution of cysteine for leucine at position 201, encoded by pilTL201C). Purified PilTL201C forms a native hexamer, but mutant hexamers hydrolyze ATP at half the maximal rate. N. gonorrhoeae pilTL201C cells produce Tfp fibers, crawl at the same speed as the wild-type (wt) parent, and are equally transformable. However, the social behavior of pilTL201C cells is intermediate between the behaviors of wt and ΔpilT cells. The infection behavior of pilTL201C is also defective, due to its failure to activate the epidermal growth factor receptor (EGFR)-heparin-binding EGF-like growth factor (HB-EGF) pathway. Our study indicates that pilus retraction, per se, is not sufficient for N. gonorrhoeae microcolony formation or infectivity; rather, these activities are sensitive to the strength of PilT enzymatic activity. We discuss the implications of these findings for Neisseria pathogenesis in the context of mechanobiology. IMPORTANCE Type IV pili are fibers expressed on the surface of many bacteria. Neisseria gonorrhoeae cells crawl, take up DNA, and communicate with each other and with human cells by retracting these fibers. Here, we show that an N. gonorrhoeae mutant expressing an enzymatically weakened type IV pilus retraction motor still crawls and takes up DNA normally. However, mutant cells exhibit abnormal social behavior, and they are less infective because they fail to activate the epidermal growth factor receptor. Our study shows that N. gonorrhoeae social and infection behaviors are sensitive to the strength of the retraction motor enzyme.
format	article
author	Alyson M. Hockenberry Danielle M. Hutchens Al Agellon Magdalene So
author_facet	Alyson M. Hockenberry Danielle M. Hutchens Al Agellon Magdalene So
author_sort	Alyson M. Hockenberry
title	Attenuation of the Type IV Pilus Retraction Motor Influences <named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Social and Infection Behavior
title_short	Attenuation of the Type IV Pilus Retraction Motor Influences <named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Social and Infection Behavior
title_full	Attenuation of the Type IV Pilus Retraction Motor Influences <named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Social and Infection Behavior
title_fullStr	Attenuation of the Type IV Pilus Retraction Motor Influences <named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Social and Infection Behavior
title_full_unstemmed	Attenuation of the Type IV Pilus Retraction Motor Influences <named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Social and Infection Behavior
title_sort	attenuation of the type iv pilus retraction motor influences <named-content content-type="genus-species">neisseria gonorrhoeae</named-content> social and infection behavior
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/e5ea5d8d9b66451d8a8311baf10459a3
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Attenuation of the Type IV Pilus Retraction Motor Influences <named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Social and Infection Behavior

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