The Characteristics and Expression Profile of Peptidoglycan Recognition Protein 2 in the Accessory Nidamental Gland of the Bigfin Reef Squid During Bacterial Colonization

Some cephalopods carry microorganisms in two specialized organs, the light organ and the accessory nidamental gland (ANG). For the light organ, comprehensive mechanisms have been described for winnowing (bacterial selection) and maintenance of the symbiotic luminescent bacterium Vibrio fischeri (V....

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Main Authors: Hau-Wen Li, Wei-Lun Kuo, Chi Chen, Yung-Che Tseng, Ching-Fong Chang, Guan-Chung Wu
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2022.825267/full
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author Hau-Wen Li
Wei-Lun Kuo
Chi Chen
Chi Chen
Yung-Che Tseng
Ching-Fong Chang
Ching-Fong Chang
Guan-Chung Wu
Guan-Chung Wu
author_facet Hau-Wen Li
Wei-Lun Kuo
Chi Chen
Chi Chen
Yung-Che Tseng
Ching-Fong Chang
Ching-Fong Chang
Guan-Chung Wu
Guan-Chung Wu
author_sort Hau-Wen Li
collection DOAJ
description Some cephalopods carry microorganisms in two specialized organs, the light organ and the accessory nidamental gland (ANG). For the light organ, comprehensive mechanisms have been described for winnowing (bacterial selection) and maintenance of the symbiotic luminescent bacterium Vibrio fischeri (V. fischeri). However, the mechanisms controlling bacterial selection and maintenance during bacterial colonization of the ANG are open biological issues with physiological significance. Our recent study on bigfin reef squid (Sepioteuthis lessoniana) already showed that the ANG bacterial community shifts gradually and exhibits decreased diversity throughout maturation. This study further describes a potential role of an innate immunity-involved molecule, peptidoglycan recognition proteins (PGRPs), in the ANG of bigfin reef squid during bacterial transmission and colonization. First, we found that four homologs of the PGRP family are expressed in the ANG of bigfin reef squid (slPGRP2-5), but only slPgrp2 transcript levels are highly correlated with ANG development and bacterial colonization. Besides, slPgrp2 transcripts are mainly expressed in the epithelial cells of certain secondary tubules of ANG, and the expression levels are varied in the epithelial cells of other secondary tubules. This data reveals that slPgrp2 transcripts may associate with the composition of bacterial consortium and its secretary factors. Moreover, recombinant slPGRP2 had a negative effect of Escherichia coli (E.coli) which inhibited bacterial growth in culture. Therefore, our data suggest slPgrp2 expression in the epithelial cells of secondary tubules in the ANG may have an essential role in the winnowing and maintenance of holobiont homeostasis in bigfin reef squid.
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spelling doaj.art-1f68a0edcd9a4026b2bf812ee1c3d8092022-12-22T00:37:33ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452022-05-01910.3389/fmars.2022.825267825267The Characteristics and Expression Profile of Peptidoglycan Recognition Protein 2 in the Accessory Nidamental Gland of the Bigfin Reef Squid During Bacterial ColonizationHau-Wen Li0Wei-Lun Kuo1Chi Chen2Chi Chen3Yung-Che Tseng4Ching-Fong Chang5Ching-Fong Chang6Guan-Chung Wu7Guan-Chung Wu8Department of Aquaculture, National Taiwan Ocean University, Keelung, TaiwanDepartment of Aquaculture, National Taiwan Ocean University, Keelung, TaiwanDoctoral Degree Program in Marine Biotechnology, National Taiwan Ocean University, Keelung, TaiwanDoctoral Degree Program in Marine Biotechnology, Academia Sinica, Taipei, TaiwanMarine Research Station, Institute of Cellular and Organismic Biology, Academia Sinica, Taipei, TaiwanDepartment of Aquaculture, National Taiwan Ocean University, Keelung, TaiwanCenter of Excellence for the Oceans, National Taiwan Ocean University, Keelung, TaiwanDepartment of Aquaculture, National Taiwan Ocean University, Keelung, TaiwanCenter of Excellence for the Oceans, National Taiwan Ocean University, Keelung, TaiwanSome cephalopods carry microorganisms in two specialized organs, the light organ and the accessory nidamental gland (ANG). For the light organ, comprehensive mechanisms have been described for winnowing (bacterial selection) and maintenance of the symbiotic luminescent bacterium Vibrio fischeri (V. fischeri). However, the mechanisms controlling bacterial selection and maintenance during bacterial colonization of the ANG are open biological issues with physiological significance. Our recent study on bigfin reef squid (Sepioteuthis lessoniana) already showed that the ANG bacterial community shifts gradually and exhibits decreased diversity throughout maturation. This study further describes a potential role of an innate immunity-involved molecule, peptidoglycan recognition proteins (PGRPs), in the ANG of bigfin reef squid during bacterial transmission and colonization. First, we found that four homologs of the PGRP family are expressed in the ANG of bigfin reef squid (slPGRP2-5), but only slPgrp2 transcript levels are highly correlated with ANG development and bacterial colonization. Besides, slPgrp2 transcripts are mainly expressed in the epithelial cells of certain secondary tubules of ANG, and the expression levels are varied in the epithelial cells of other secondary tubules. This data reveals that slPgrp2 transcripts may associate with the composition of bacterial consortium and its secretary factors. Moreover, recombinant slPGRP2 had a negative effect of Escherichia coli (E.coli) which inhibited bacterial growth in culture. Therefore, our data suggest slPgrp2 expression in the epithelial cells of secondary tubules in the ANG may have an essential role in the winnowing and maintenance of holobiont homeostasis in bigfin reef squid.https://www.frontiersin.org/articles/10.3389/fmars.2022.825267/fullPGRPhost immunitysymbiotic bacteriaANGcephalopod
spellingShingle Hau-Wen Li
Wei-Lun Kuo
Chi Chen
Chi Chen
Yung-Che Tseng
Ching-Fong Chang
Ching-Fong Chang
Guan-Chung Wu
Guan-Chung Wu
The Characteristics and Expression Profile of Peptidoglycan Recognition Protein 2 in the Accessory Nidamental Gland of the Bigfin Reef Squid During Bacterial Colonization
Frontiers in Marine Science
PGRP
host immunity
symbiotic bacteria
ANG
cephalopod
title The Characteristics and Expression Profile of Peptidoglycan Recognition Protein 2 in the Accessory Nidamental Gland of the Bigfin Reef Squid During Bacterial Colonization
title_full The Characteristics and Expression Profile of Peptidoglycan Recognition Protein 2 in the Accessory Nidamental Gland of the Bigfin Reef Squid During Bacterial Colonization
title_fullStr The Characteristics and Expression Profile of Peptidoglycan Recognition Protein 2 in the Accessory Nidamental Gland of the Bigfin Reef Squid During Bacterial Colonization
title_full_unstemmed The Characteristics and Expression Profile of Peptidoglycan Recognition Protein 2 in the Accessory Nidamental Gland of the Bigfin Reef Squid During Bacterial Colonization
title_short The Characteristics and Expression Profile of Peptidoglycan Recognition Protein 2 in the Accessory Nidamental Gland of the Bigfin Reef Squid During Bacterial Colonization
title_sort characteristics and expression profile of peptidoglycan recognition protein 2 in the accessory nidamental gland of the bigfin reef squid during bacterial colonization
topic PGRP
host immunity
symbiotic bacteria
ANG
cephalopod
url https://www.frontiersin.org/articles/10.3389/fmars.2022.825267/full
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