Community changes of gut microbes highlight their importance in the adaptation of copepods to toxic dinoflagellates

Zooplankton grazers, like copepods, can feed on toxic microalgae and live normally. We hypothesize that gut microbial communities (GMCs) may contribute to the detoxification of the host by changing their compositions and recruiting more beneficial bacteria. Here, we measured the physiological respon...

Full description

Bibliographic Details
Main Authors: Jing Yang, Zhimeng Xu, Yi Chen, Huo Xu, Zuyuan Gao, Xiaodong Zhang, Mengwen Pang, Shuwen Zhang, Hongbin Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-04-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2024.1368315/full
_version_ 1827292661143306240
author Jing Yang
Zhimeng Xu
Yi Chen
Huo Xu
Zuyuan Gao
Xiaodong Zhang
Mengwen Pang
Shuwen Zhang
Hongbin Liu
Hongbin Liu
author_facet Jing Yang
Zhimeng Xu
Yi Chen
Huo Xu
Zuyuan Gao
Xiaodong Zhang
Mengwen Pang
Shuwen Zhang
Hongbin Liu
Hongbin Liu
author_sort Jing Yang
collection DOAJ
description Zooplankton grazers, like copepods, can feed on toxic microalgae and live normally. We hypothesize that gut microbial communities (GMCs) may contribute to the detoxification of the host by changing their compositions and recruiting more beneficial bacteria. Here, we measured the physiological responses of two copepod species (Acartia sp. and Paracalanus sp.) fed with toxic (Alexandrium tamarense) and non-toxic (Alexandrium andersonii) dinoflagellates, respectively. Both copepods maintained consistently high survival rates but slightly reduced ingestion rates when feeding upon the toxic dinoflagellate (when compared to the non-toxic one), suggesting a compensatory mechanism. The compositional variation of copepod GMCs, at the amplicon sequence variant (ASV) level, was mostly significantly different among copepod host species (R = 0.83, by ANOSIM test), while diet type played minor but significant roles. Under the toxic diet, Acartia sp. enriched only five ASVs while Paracalanus sp. recruited a wide range of taxa (38 ASVs) mostly belonging to Alphaproteobacteria (e.g., Rhodobacteraceae) and Gammaproteobacteria (e.g., Alteromonadaceae). In contrast, when clustering GMCs by predicted functions, diet type was the key regulating factor, suggesting the functional convergence of copepod GMCs in response to algal toxins. This can be explained by the fact that most of the enriched bacteria under the toxic diet have similar functions on detoxification and maintaining the host homeostasis. This study deepens our understanding of the roles of GMC in the detoxification and adaptation mechanisms of copepods during harmful algal blooms.
first_indexed 2024-04-24T13:09:41Z
format Article
id doaj.art-7a54c8848a824460837b311ea27bd5a5
institution Directory Open Access Journal
issn 2296-7745
language English
last_indexed 2024-04-24T13:09:41Z
publishDate 2024-04-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Marine Science
spelling doaj.art-7a54c8848a824460837b311ea27bd5a52024-04-05T04:59:36ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452024-04-011110.3389/fmars.2024.13683151368315Community changes of gut microbes highlight their importance in the adaptation of copepods to toxic dinoflagellatesJing Yang0Zhimeng Xu1Yi Chen2Huo Xu3Zuyuan Gao4Xiaodong Zhang5Mengwen Pang6Shuwen Zhang7Hongbin Liu8Hongbin Liu9Department of Ocean Science, The Hong Kong University of Science and Technology, Hong Kong SAR, ChinaDepartment of Ocean Science, The Hong Kong University of Science and Technology, Hong Kong SAR, ChinaDepartment of Ocean Science, The Hong Kong University of Science and Technology, Hong Kong SAR, ChinaDepartment of Ocean Science, The Hong Kong University of Science and Technology, Hong Kong SAR, ChinaDepartment of Ocean Science, The Hong Kong University of Science and Technology, Hong Kong SAR, ChinaDepartment of Ocean Science, The Hong Kong University of Science and Technology, Hong Kong SAR, ChinaDepartment of Ocean Science, The Hong Kong University of Science and Technology, Hong Kong SAR, ChinaGuangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Science, South China Normal University, Guangzhou, ChinaDepartment of Ocean Science, The Hong Kong University of Science and Technology, Hong Kong SAR, ChinaHong Kong Branch of the Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), The Hong Kong University of Science and Technology, Hong Kong, Hong Kong SAR, ChinaZooplankton grazers, like copepods, can feed on toxic microalgae and live normally. We hypothesize that gut microbial communities (GMCs) may contribute to the detoxification of the host by changing their compositions and recruiting more beneficial bacteria. Here, we measured the physiological responses of two copepod species (Acartia sp. and Paracalanus sp.) fed with toxic (Alexandrium tamarense) and non-toxic (Alexandrium andersonii) dinoflagellates, respectively. Both copepods maintained consistently high survival rates but slightly reduced ingestion rates when feeding upon the toxic dinoflagellate (when compared to the non-toxic one), suggesting a compensatory mechanism. The compositional variation of copepod GMCs, at the amplicon sequence variant (ASV) level, was mostly significantly different among copepod host species (R = 0.83, by ANOSIM test), while diet type played minor but significant roles. Under the toxic diet, Acartia sp. enriched only five ASVs while Paracalanus sp. recruited a wide range of taxa (38 ASVs) mostly belonging to Alphaproteobacteria (e.g., Rhodobacteraceae) and Gammaproteobacteria (e.g., Alteromonadaceae). In contrast, when clustering GMCs by predicted functions, diet type was the key regulating factor, suggesting the functional convergence of copepod GMCs in response to algal toxins. This can be explained by the fact that most of the enriched bacteria under the toxic diet have similar functions on detoxification and maintaining the host homeostasis. This study deepens our understanding of the roles of GMC in the detoxification and adaptation mechanisms of copepods during harmful algal blooms.https://www.frontiersin.org/articles/10.3389/fmars.2024.1368315/fullharmful algal bloomsdinoflagellatescopepodsgut microbesdetoxificationtoxic microalgae
spellingShingle Jing Yang
Zhimeng Xu
Yi Chen
Huo Xu
Zuyuan Gao
Xiaodong Zhang
Mengwen Pang
Shuwen Zhang
Hongbin Liu
Hongbin Liu
Community changes of gut microbes highlight their importance in the adaptation of copepods to toxic dinoflagellates
Frontiers in Marine Science
harmful algal blooms
dinoflagellates
copepods
gut microbes
detoxification
toxic microalgae
title Community changes of gut microbes highlight their importance in the adaptation of copepods to toxic dinoflagellates
title_full Community changes of gut microbes highlight their importance in the adaptation of copepods to toxic dinoflagellates
title_fullStr Community changes of gut microbes highlight their importance in the adaptation of copepods to toxic dinoflagellates
title_full_unstemmed Community changes of gut microbes highlight their importance in the adaptation of copepods to toxic dinoflagellates
title_short Community changes of gut microbes highlight their importance in the adaptation of copepods to toxic dinoflagellates
title_sort community changes of gut microbes highlight their importance in the adaptation of copepods to toxic dinoflagellates
topic harmful algal blooms
dinoflagellates
copepods
gut microbes
detoxification
toxic microalgae
url https://www.frontiersin.org/articles/10.3389/fmars.2024.1368315/full
work_keys_str_mv AT jingyang communitychangesofgutmicrobeshighlighttheirimportanceintheadaptationofcopepodstotoxicdinoflagellates
AT zhimengxu communitychangesofgutmicrobeshighlighttheirimportanceintheadaptationofcopepodstotoxicdinoflagellates
AT yichen communitychangesofgutmicrobeshighlighttheirimportanceintheadaptationofcopepodstotoxicdinoflagellates
AT huoxu communitychangesofgutmicrobeshighlighttheirimportanceintheadaptationofcopepodstotoxicdinoflagellates
AT zuyuangao communitychangesofgutmicrobeshighlighttheirimportanceintheadaptationofcopepodstotoxicdinoflagellates
AT xiaodongzhang communitychangesofgutmicrobeshighlighttheirimportanceintheadaptationofcopepodstotoxicdinoflagellates
AT mengwenpang communitychangesofgutmicrobeshighlighttheirimportanceintheadaptationofcopepodstotoxicdinoflagellates
AT shuwenzhang communitychangesofgutmicrobeshighlighttheirimportanceintheadaptationofcopepodstotoxicdinoflagellates
AT hongbinliu communitychangesofgutmicrobeshighlighttheirimportanceintheadaptationofcopepodstotoxicdinoflagellates
AT hongbinliu communitychangesofgutmicrobeshighlighttheirimportanceintheadaptationofcopepodstotoxicdinoflagellates