Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defense

Detalhes bibliográficos
Autor(a) principal: Greenspan, Sasha E.
Data de Publicação: 2019
Outros Autores: Lyra, Mariana L. [UNESP], Migliorini, Gustavo H. [UNESP], Kersch-Becker, Monica F., Bletz, Molly C., Lisboa, Cybele Sabino, Pontes, Mariana R., Ribeiro, Luisa P., Neely, Wesley J., Rezende, Felipe, Romero, Gustavo Q., Woodhams, Douglas C., Haddad, Celio F. B. [UNESP], Toledo, Luis Felipe, Becker, C. Guilherme
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1098/rspb.2019.0924
http://hdl.handle.net/11449/185864
Resumo: The host-associated microbiome is vital to host immunity and pathogen defense. In aquatic ecosystems, organisms may interact with environmental bacteria to influence the pool of potential symbionts, but the effects of these interactions on host microbiome assembly and pathogen resistance are unresolved. We used replicated bromeliad microecosystems to test for indirect effects of arthropod-bacteria interactions on host microbiome assembly and pathogen burden, using tadpoles and the fungal amphibian pathogen Batrachochytrium dendrobatidis as a model host-pathogen system. Arthropods influenced host microbiome assembly by altering the pool of environmental bacteria, with arthropod-bacteria interactions specifically reducing host colonization by transient bacteria and promoting antimicrobial components of aquatic bacterial communities. Arthropods also reduced fungal zoospores in the environment, but fungal infection burdens in tadpoles corresponded most closely with arthropod-mediated patterns in microbiome assembly. This result indicates that the cascading effects of arthropods on the maintenance of a protective host microbiome may be more strongly linked to host health than negative effects of arthropods on pools of pathogenic zoospores. Our work reveals tight links between healthy ecosystem dynamics and the functioning of host microbiomes, suggesting that ecosystem disturbances such as loss of arthropods may have downstream effects on host-associated microbial pathogen defenses and host fitness.
id UNSP_91a8d988d7fafaefb13c2e74c70f773d
oai_identifier_str oai:repositorio.unesp.br:11449/185864
network_acronym_str UNSP
network_name_str Repositório Institucional da UNESP
repository_id_str 2946
spelling Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defenseamphibianarthropodBatrachochytrium dendrobatidischytridiomycosisdiseasehost microbiomeThe host-associated microbiome is vital to host immunity and pathogen defense. In aquatic ecosystems, organisms may interact with environmental bacteria to influence the pool of potential symbionts, but the effects of these interactions on host microbiome assembly and pathogen resistance are unresolved. We used replicated bromeliad microecosystems to test for indirect effects of arthropod-bacteria interactions on host microbiome assembly and pathogen burden, using tadpoles and the fungal amphibian pathogen Batrachochytrium dendrobatidis as a model host-pathogen system. Arthropods influenced host microbiome assembly by altering the pool of environmental bacteria, with arthropod-bacteria interactions specifically reducing host colonization by transient bacteria and promoting antimicrobial components of aquatic bacterial communities. Arthropods also reduced fungal zoospores in the environment, but fungal infection burdens in tadpoles corresponded most closely with arthropod-mediated patterns in microbiome assembly. This result indicates that the cascading effects of arthropods on the maintenance of a protective host microbiome may be more strongly linked to host health than negative effects of arthropods on pools of pathogenic zoospores. Our work reveals tight links between healthy ecosystem dynamics and the functioning of host microbiomes, suggesting that ecosystem disturbances such as loss of arthropods may have downstream effects on host-associated microbial pathogen defenses and host fitness.Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)Univ Alabama, Dept Biol Sci, Tuscaloosa, AL 35487 USAUniv Estadual Paulista, Dept Zool, BR-13506900 Rio Claro, SP, BrazilUniv Estadual Paulista, Aquaculture Ctr CAUNESP, BR-13506900 Rio Claro, SP, BrazilUniv Estadual Paulista, Programa Posgrad Biol Anim, BR-15054000 Sao Jose Do Rio Preto, SP, BrazilUniv Massachusetts, Dept Biol, Boston, MA 02125 USAFundacao Parque Zool Sao Paulo, BR-04301905 Sao Paulo, SP, BrazilUniv Estadual Campinas, Inst Biol, Programa Posgrad Ecol, BR-13083862 Campinas, SP, BrazilUniv Estadual Campinas, Dept Biol Anim, BR-13083862 Campinas, SP, BrazilUniv Estadual Campinas, Dept Biol Anim, Lab Hist Nat Anfibios Brasileiros LaHNAB, BR-13083862 Campinas, SP, BrazilUniv Estadual Paulista, Dept Zool, BR-13506900 Rio Claro, SP, BrazilUniv Estadual Paulista, Aquaculture Ctr CAUNESP, BR-13506900 Rio Claro, SP, BrazilUniv Estadual Paulista, Programa Posgrad Biol Anim, BR-15054000 Sao Jose Do Rio Preto, SP, BrazilFAPESP: 2014/23388-7FAPESP: 2013/50741-7FAPESP: 2014/50342-8FAPESP: 2017/26162-8FAPESP: 2016/03344-0CNPq: 312895/2014-3CNPq: 300896/2016-6CNPq: 302518/2013-4CAPES: 001Royal SocUniv AlabamaUniversidade Estadual Paulista (Unesp)Univ MassachusettsFundacao Parque Zool Sao PauloUniversidade Estadual de Campinas (UNICAMP)Greenspan, Sasha E.Lyra, Mariana L. [UNESP]Migliorini, Gustavo H. [UNESP]Kersch-Becker, Monica F.Bletz, Molly C.Lisboa, Cybele SabinoPontes, Mariana R.Ribeiro, Luisa P.Neely, Wesley J.Rezende, FelipeRomero, Gustavo Q.Woodhams, Douglas C.Haddad, Celio F. B. [UNESP]Toledo, Luis FelipeBecker, C. Guilherme2019-10-04T12:39:13Z2019-10-04T12:39:13Z2019-06-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/article10http://dx.doi.org/10.1098/rspb.2019.0924Proceedings Of The Royal Society B-biological Sciences. London: Royal Soc, v. 286, n. 1905, 10 p., 2019.0962-8452http://hdl.handle.net/11449/18586410.1098/rspb.2019.0924WOS:000473752400008Web of Sciencereponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengProceedings Of The Royal Society B-biological Sciencesinfo:eu-repo/semantics/openAccess2021-10-22T21:15:49Zoai:repositorio.unesp.br:11449/185864Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T19:24:24.583089Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defense
title Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defense
spellingShingle Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defense
Greenspan, Sasha E.
amphibian
arthropod
Batrachochytrium dendrobatidis
chytridiomycosis
disease
host microbiome
title_short Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defense
title_full Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defense
title_fullStr Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defense
title_full_unstemmed Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defense
title_sort Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defense
author Greenspan, Sasha E.
author_facet Greenspan, Sasha E.
Lyra, Mariana L. [UNESP]
Migliorini, Gustavo H. [UNESP]
Kersch-Becker, Monica F.
Bletz, Molly C.
Lisboa, Cybele Sabino
Pontes, Mariana R.
Ribeiro, Luisa P.
Neely, Wesley J.
Rezende, Felipe
Romero, Gustavo Q.
Woodhams, Douglas C.
Haddad, Celio F. B. [UNESP]
Toledo, Luis Felipe
Becker, C. Guilherme
author_role author
author2 Lyra, Mariana L. [UNESP]
Migliorini, Gustavo H. [UNESP]
Kersch-Becker, Monica F.
Bletz, Molly C.
Lisboa, Cybele Sabino
Pontes, Mariana R.
Ribeiro, Luisa P.
Neely, Wesley J.
Rezende, Felipe
Romero, Gustavo Q.
Woodhams, Douglas C.
Haddad, Celio F. B. [UNESP]
Toledo, Luis Felipe
Becker, C. Guilherme
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Univ Alabama
Universidade Estadual Paulista (Unesp)
Univ Massachusetts
Fundacao Parque Zool Sao Paulo
Universidade Estadual de Campinas (UNICAMP)
dc.contributor.author.fl_str_mv Greenspan, Sasha E.
Lyra, Mariana L. [UNESP]
Migliorini, Gustavo H. [UNESP]
Kersch-Becker, Monica F.
Bletz, Molly C.
Lisboa, Cybele Sabino
Pontes, Mariana R.
Ribeiro, Luisa P.
Neely, Wesley J.
Rezende, Felipe
Romero, Gustavo Q.
Woodhams, Douglas C.
Haddad, Celio F. B. [UNESP]
Toledo, Luis Felipe
Becker, C. Guilherme
dc.subject.por.fl_str_mv amphibian
arthropod
Batrachochytrium dendrobatidis
chytridiomycosis
disease
host microbiome
topic amphibian
arthropod
Batrachochytrium dendrobatidis
chytridiomycosis
disease
host microbiome
description The host-associated microbiome is vital to host immunity and pathogen defense. In aquatic ecosystems, organisms may interact with environmental bacteria to influence the pool of potential symbionts, but the effects of these interactions on host microbiome assembly and pathogen resistance are unresolved. We used replicated bromeliad microecosystems to test for indirect effects of arthropod-bacteria interactions on host microbiome assembly and pathogen burden, using tadpoles and the fungal amphibian pathogen Batrachochytrium dendrobatidis as a model host-pathogen system. Arthropods influenced host microbiome assembly by altering the pool of environmental bacteria, with arthropod-bacteria interactions specifically reducing host colonization by transient bacteria and promoting antimicrobial components of aquatic bacterial communities. Arthropods also reduced fungal zoospores in the environment, but fungal infection burdens in tadpoles corresponded most closely with arthropod-mediated patterns in microbiome assembly. This result indicates that the cascading effects of arthropods on the maintenance of a protective host microbiome may be more strongly linked to host health than negative effects of arthropods on pools of pathogenic zoospores. Our work reveals tight links between healthy ecosystem dynamics and the functioning of host microbiomes, suggesting that ecosystem disturbances such as loss of arthropods may have downstream effects on host-associated microbial pathogen defenses and host fitness.
publishDate 2019
dc.date.none.fl_str_mv 2019-10-04T12:39:13Z
2019-10-04T12:39:13Z
2019-06-01
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1098/rspb.2019.0924
Proceedings Of The Royal Society B-biological Sciences. London: Royal Soc, v. 286, n. 1905, 10 p., 2019.
0962-8452
http://hdl.handle.net/11449/185864
10.1098/rspb.2019.0924
WOS:000473752400008
url http://dx.doi.org/10.1098/rspb.2019.0924
http://hdl.handle.net/11449/185864
identifier_str_mv Proceedings Of The Royal Society B-biological Sciences. London: Royal Soc, v. 286, n. 1905, 10 p., 2019.
0962-8452
10.1098/rspb.2019.0924
WOS:000473752400008
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Proceedings Of The Royal Society B-biological Sciences
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 10
dc.publisher.none.fl_str_mv Royal Soc
publisher.none.fl_str_mv Royal Soc
dc.source.none.fl_str_mv Web of Science
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
repository.mail.fl_str_mv
_version_ 1808129063300104192