Modulation of Symbiont Lipid A Signaling by Host Alkaline Phosphatases in the Squid-Vibrio Symbiosis

ABSTRACT The synergistic activity of Vibrio fischeri lipid A and the peptidoglycan monomer (tracheal cytotoxin [TCT]) induces apoptosis in the superficial cells of the juvenile Euprymna scolopes light organ during the onset of the squid-vibrio symbiosis. Once the association is established in the ep...

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Autores principales:	Bethany A. Rader, Natacha Kremer, Michael A. Apicella, William E. Goldman, Margaret J. McFall-Ngai
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2012
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b4c40780a772443883079a13da54daf0
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spelling	oai:doaj.org-article:b4c40780a772443883079a13da54daf02021-11-15T15:39:01ZModulation of Symbiont Lipid A Signaling by Host Alkaline Phosphatases in the Squid-Vibrio Symbiosis10.1128/mBio.00093-122150-7511https://doaj.org/article/b4c40780a772443883079a13da54daf02012-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00093-12https://doaj.org/toc/2150-7511ABSTRACT The synergistic activity of Vibrio fischeri lipid A and the peptidoglycan monomer (tracheal cytotoxin [TCT]) induces apoptosis in the superficial cells of the juvenile Euprymna scolopes light organ during the onset of the squid-vibrio symbiosis. Once the association is established in the epithelium-lined crypts of the light organ, the host degrades the symbiont’s constitutively produced TCT by the amidase activity of a peptidoglycan recognition protein (E. scolopes peptidoglycan recognition protein 2 [EsPGRP2]). In the present study, we explored the role of alkaline phosphatases in transforming the lipid A of the symbiont into a form that changes its signaling properties to host tissues. We obtained full-length open reading frames for two E. scolopes alkaline phosphatase (EsAP) mRNAs (esap1 and esap2); transcript levels suggested that the dominant light organ isoform is EsAP1. Levels of total EsAP activity increased with symbiosis, but only after the lipid A-dependent morphogenetic induction at 12 h, and were regulated over the day-night cycle. Inhibition of total EsAP activity impaired normal colonization and persistence by the symbiont. EsAP activity localized to the internal regions of the symbiotic juvenile light organ, including the lumina of the crypt spaces where the symbiont resides. These data provide evidence that EsAPs work in concert with EsPGRPs to change the signaling properties of bacterial products and thereby promote persistent colonization by the mutualistic symbiont. IMPORTANCE The potential for microbe-associated molecular patterns (MAMPs) to compromise host-tissue health is reflected in the often-used nomenclature for these molecules: lipopolysaccharide (LPS) is also called “endotoxin” and the peptidoglycan monomer is also called “tracheal cytotoxin” (TCT). With constant presentation of MAMPs by the normal microbiota, mechanisms to tolerate their effects have developed. The results of this contribution provide evidence that host alkaline phosphatases (APs) dephosphorylate and inactivate the symbiont MAMP lipid A. As such, APs work in synergy with a peptidoglycan recognition protein, which inactivates symbiont-exported TCT, to alter the symbiont MAMPs and promote persistence of the partnership. Not only may these activities serve to “tame” the MAMPs, but also the resulting products may themselves be important signals in persistent mutualisms. The finding of lipid A modification by APs in an invertebrate mutualism provides evidence that this specific strategy for dealing with symbiotic partners is conserved across the animal kingdom.Bethany A. RaderNatacha KremerMichael A. ApicellaWilliam E. GoldmanMargaret J. McFall-NgaiAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 3 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Bethany A. Rader Natacha Kremer Michael A. Apicella William E. Goldman Margaret J. McFall-Ngai Modulation of Symbiont Lipid A Signaling by Host Alkaline Phosphatases in the Squid-Vibrio Symbiosis
description	ABSTRACT The synergistic activity of Vibrio fischeri lipid A and the peptidoglycan monomer (tracheal cytotoxin [TCT]) induces apoptosis in the superficial cells of the juvenile Euprymna scolopes light organ during the onset of the squid-vibrio symbiosis. Once the association is established in the epithelium-lined crypts of the light organ, the host degrades the symbiont’s constitutively produced TCT by the amidase activity of a peptidoglycan recognition protein (E. scolopes peptidoglycan recognition protein 2 [EsPGRP2]). In the present study, we explored the role of alkaline phosphatases in transforming the lipid A of the symbiont into a form that changes its signaling properties to host tissues. We obtained full-length open reading frames for two E. scolopes alkaline phosphatase (EsAP) mRNAs (esap1 and esap2); transcript levels suggested that the dominant light organ isoform is EsAP1. Levels of total EsAP activity increased with symbiosis, but only after the lipid A-dependent morphogenetic induction at 12 h, and were regulated over the day-night cycle. Inhibition of total EsAP activity impaired normal colonization and persistence by the symbiont. EsAP activity localized to the internal regions of the symbiotic juvenile light organ, including the lumina of the crypt spaces where the symbiont resides. These data provide evidence that EsAPs work in concert with EsPGRPs to change the signaling properties of bacterial products and thereby promote persistent colonization by the mutualistic symbiont. IMPORTANCE The potential for microbe-associated molecular patterns (MAMPs) to compromise host-tissue health is reflected in the often-used nomenclature for these molecules: lipopolysaccharide (LPS) is also called “endotoxin” and the peptidoglycan monomer is also called “tracheal cytotoxin” (TCT). With constant presentation of MAMPs by the normal microbiota, mechanisms to tolerate their effects have developed. The results of this contribution provide evidence that host alkaline phosphatases (APs) dephosphorylate and inactivate the symbiont MAMP lipid A. As such, APs work in synergy with a peptidoglycan recognition protein, which inactivates symbiont-exported TCT, to alter the symbiont MAMPs and promote persistence of the partnership. Not only may these activities serve to “tame” the MAMPs, but also the resulting products may themselves be important signals in persistent mutualisms. The finding of lipid A modification by APs in an invertebrate mutualism provides evidence that this specific strategy for dealing with symbiotic partners is conserved across the animal kingdom.
format	article
author	Bethany A. Rader Natacha Kremer Michael A. Apicella William E. Goldman Margaret J. McFall-Ngai
author_facet	Bethany A. Rader Natacha Kremer Michael A. Apicella William E. Goldman Margaret J. McFall-Ngai
author_sort	Bethany A. Rader
title	Modulation of Symbiont Lipid A Signaling by Host Alkaline Phosphatases in the Squid-Vibrio Symbiosis
title_short	Modulation of Symbiont Lipid A Signaling by Host Alkaline Phosphatases in the Squid-Vibrio Symbiosis
title_full	Modulation of Symbiont Lipid A Signaling by Host Alkaline Phosphatases in the Squid-Vibrio Symbiosis
title_fullStr	Modulation of Symbiont Lipid A Signaling by Host Alkaline Phosphatases in the Squid-Vibrio Symbiosis
title_full_unstemmed	Modulation of Symbiont Lipid A Signaling by Host Alkaline Phosphatases in the Squid-Vibrio Symbiosis
title_sort	modulation of symbiont lipid a signaling by host alkaline phosphatases in the squid-vibrio symbiosis
publisher	American Society for Microbiology
publishDate	2012
url	https://doaj.org/article/b4c40780a772443883079a13da54daf0
work_keys_str_mv	AT bethanyarader modulationofsymbiontlipidasignalingbyhostalkalinephosphatasesinthesquidvibriosymbiosis AT natachakremer modulationofsymbiontlipidasignalingbyhostalkalinephosphatasesinthesquidvibriosymbiosis AT michaelaapicella modulationofsymbiontlipidasignalingbyhostalkalinephosphatasesinthesquidvibriosymbiosis AT williamegoldman modulationofsymbiontlipidasignalingbyhostalkalinephosphatasesinthesquidvibriosymbiosis AT margaretjmcfallngai modulationofsymbiontlipidasignalingbyhostalkalinephosphatasesinthesquidvibriosymbiosis
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Modulation of Symbiont Lipid A Signaling by Host Alkaline Phosphatases in the Squid-Vibrio Symbiosis

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