Dynamic evolution of the LPS-detoxifying enzyme intestinal alkaline phosphatase in zebrafish and other vertebrates

Alkaline phosphatases (Alps) are well-studied enzymes that remove phosphates from a variety of substrates. Alps function in diverse biological processes, including modulating host-bacterial interactions by dephosphorylating the Gram-negative bacterial cell wall component lipopolysaccharide (LPS). In...

Full description

Bibliographic Details
Main Authors: Ye eYang, Anica M Wandler, John H Postlethwait, Karen eGuillemin
Format: Article
Language:English
Published: Frontiers Media S.A. 2012-10-01
Series:Frontiers in Immunology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fimmu.2012.00314/full
_version_ 1818110459529658368
author Ye eYang
Anica M Wandler
John H Postlethwait
Karen eGuillemin
author_facet Ye eYang
Anica M Wandler
John H Postlethwait
Karen eGuillemin
author_sort Ye eYang
collection DOAJ
description Alkaline phosphatases (Alps) are well-studied enzymes that remove phosphates from a variety of substrates. Alps function in diverse biological processes, including modulating host-bacterial interactions by dephosphorylating the Gram-negative bacterial cell wall component lipopolysaccharide (LPS). In animals, Alps are encoded by multiple genes characterized by either ubiquitous expression (named Alpls, for their liver expression), or their tissue-specific expression, for example in the intestine (Alpi). We previously characterized a zebrafish alpi gene (renamed here alpi.1) that is regulated by Myd88-dependent innate immune signaling and that is required to prevent a host’s excessive inflammatory reactions to its resident microbiota. Here we report the characterization of two new alp genes in zebrafish, alpi.2 and alp3. To understand their origins, we investigated the phylogenetic history of Alp genes in animals. We find that vertebrate Alp genes are organized in three clades with one of these clades missing from the mammals. We present evidence that these three clades originated during the two vertebrate genome duplications. We show that in zebrafish alpl is ubiquitously expressed, as it is in mammals, whereas the other three alps are specific to the intestine. Our phylogenetic analysis reveals that in contrast to Alpl, which has been stably maintained as a single gene throughout the vertebrates, the Alpis have been lost and duplicated multiple times independently in vertebrate lineages, likely reflecting the rapid and dynamic evolution of vertebrate gut morphologies, driven by changes in bacterial associations and diet.
first_indexed 2024-12-11T02:47:29Z
format Article
id doaj.art-8774889c950e480eb635dfd23ac9eacc
institution Directory Open Access Journal
issn 1664-3224
language English
last_indexed 2024-12-11T02:47:29Z
publishDate 2012-10-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj.art-8774889c950e480eb635dfd23ac9eacc2022-12-22T01:23:24ZengFrontiers Media S.A.Frontiers in Immunology1664-32242012-10-01310.3389/fimmu.2012.0031435467Dynamic evolution of the LPS-detoxifying enzyme intestinal alkaline phosphatase in zebrafish and other vertebratesYe eYang0Anica M Wandler1John H Postlethwait2Karen eGuillemin3University of OregonUniversity of OregonUniversity of OregonUniversity of OregonAlkaline phosphatases (Alps) are well-studied enzymes that remove phosphates from a variety of substrates. Alps function in diverse biological processes, including modulating host-bacterial interactions by dephosphorylating the Gram-negative bacterial cell wall component lipopolysaccharide (LPS). In animals, Alps are encoded by multiple genes characterized by either ubiquitous expression (named Alpls, for their liver expression), or their tissue-specific expression, for example in the intestine (Alpi). We previously characterized a zebrafish alpi gene (renamed here alpi.1) that is regulated by Myd88-dependent innate immune signaling and that is required to prevent a host’s excessive inflammatory reactions to its resident microbiota. Here we report the characterization of two new alp genes in zebrafish, alpi.2 and alp3. To understand their origins, we investigated the phylogenetic history of Alp genes in animals. We find that vertebrate Alp genes are organized in three clades with one of these clades missing from the mammals. We present evidence that these three clades originated during the two vertebrate genome duplications. We show that in zebrafish alpl is ubiquitously expressed, as it is in mammals, whereas the other three alps are specific to the intestine. Our phylogenetic analysis reveals that in contrast to Alpl, which has been stably maintained as a single gene throughout the vertebrates, the Alpis have been lost and duplicated multiple times independently in vertebrate lineages, likely reflecting the rapid and dynamic evolution of vertebrate gut morphologies, driven by changes in bacterial associations and diet.http://journal.frontiersin.org/Journal/10.3389/fimmu.2012.00314/fullZebrafishevolutionmicrobiotavertebrateintestinal alkaline phosphatase
spellingShingle Ye eYang
Anica M Wandler
John H Postlethwait
Karen eGuillemin
Dynamic evolution of the LPS-detoxifying enzyme intestinal alkaline phosphatase in zebrafish and other vertebrates
Frontiers in Immunology
Zebrafish
evolution
microbiota
vertebrate
intestinal alkaline phosphatase
title Dynamic evolution of the LPS-detoxifying enzyme intestinal alkaline phosphatase in zebrafish and other vertebrates
title_full Dynamic evolution of the LPS-detoxifying enzyme intestinal alkaline phosphatase in zebrafish and other vertebrates
title_fullStr Dynamic evolution of the LPS-detoxifying enzyme intestinal alkaline phosphatase in zebrafish and other vertebrates
title_full_unstemmed Dynamic evolution of the LPS-detoxifying enzyme intestinal alkaline phosphatase in zebrafish and other vertebrates
title_short Dynamic evolution of the LPS-detoxifying enzyme intestinal alkaline phosphatase in zebrafish and other vertebrates
title_sort dynamic evolution of the lps detoxifying enzyme intestinal alkaline phosphatase in zebrafish and other vertebrates
topic Zebrafish
evolution
microbiota
vertebrate
intestinal alkaline phosphatase
url http://journal.frontiersin.org/Journal/10.3389/fimmu.2012.00314/full
work_keys_str_mv AT yeeyang dynamicevolutionofthelpsdetoxifyingenzymeintestinalalkalinephosphataseinzebrafishandothervertebrates
AT anicamwandler dynamicevolutionofthelpsdetoxifyingenzymeintestinalalkalinephosphataseinzebrafishandothervertebrates
AT johnhpostlethwait dynamicevolutionofthelpsdetoxifyingenzymeintestinalalkalinephosphataseinzebrafishandothervertebrates
AT kareneguillemin dynamicevolutionofthelpsdetoxifyingenzymeintestinalalkalinephosphataseinzebrafishandothervertebrates