The structure and dynamics of complex microbe-host interaction networks

Microbes form intricate and intimate relationships with most animals and plants, many of which are crucial for host development, health and functioning. Microbe--host symbiotic associations are poorly explored in comparison with other species interaction networks. The current paradigm on symbiosis r...

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Author: Björk, Johannes
Format: doctoral thesis
Publication Date:2016
Country:España
Institution:Universitat Politècnica de Catalunya (UPC)
Repository:UPCommons. Portal del coneixement obert de la UPC
Language:English
OAI Identifier:oai:upcommons.upc.edu:2117/96369
Online Access:https://hdl.handle.net/2117/96369
https://dx.doi.org/10.5821/dissertation-2117-96369
Access Level:Open access
Keyword:Microbiologia
Microorganismes
Àrees temàtiques de la UPC::Enginyeria civil
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oai_identifier_str oai:upcommons.upc.edu:2117/96369
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv The structure and dynamics of complex microbe-host interaction networks
title The structure and dynamics of complex microbe-host interaction networks
spellingShingle The structure and dynamics of complex microbe-host interaction networks
Björk, Johannes
Microbiologia
Microorganismes
Àrees temàtiques de la UPC::Enginyeria civil
title_short The structure and dynamics of complex microbe-host interaction networks
title_full The structure and dynamics of complex microbe-host interaction networks
title_fullStr The structure and dynamics of complex microbe-host interaction networks
title_full_unstemmed The structure and dynamics of complex microbe-host interaction networks
title_sort The structure and dynamics of complex microbe-host interaction networks
dc.creator.none.fl_str_mv Björk, Johannes
author Björk, Johannes
author_facet Björk, Johannes
author_role author
dc.contributor.none.fl_str_mv Montoya Terán, José M.
dc.subject.none.fl_str_mv Microbiologia
Microorganismes
Àrees temàtiques de la UPC::Enginyeria civil
topic Microbiologia
Microorganismes
Àrees temàtiques de la UPC::Enginyeria civil
description Microbes form intricate and intimate relationships with most animals and plants, many of which are crucial for host development, health and functioning. Microbe--host symbiotic associations are poorly explored in comparison with other species interaction networks. The current paradigm on symbiosis research stems from species-poor systems where pairwise and reciprocally specialised interactions between a single microbe and host that coevolve are the norm. These symbioses involving just a few species are fascinating in their own right, but more diverse and complex host-associated microbial communities, so-called microbiomes, are increasingly found, with new emerging questions that require new paradigms and approaches. In this thesis, I investigate the structure and dynamics of complex microbe-host systems, focusing on the specialisation of their ecological interactions and on identifying fingerprints of coevolution in multispecies communities. I take a holistic approach to study interactions between complex assemblages of microbes associated to multiple host species through time and space. My overreaching objective is twofold. First, to determine the structure and dynamics of host-associated cores--a set of highly specialised and complementary microbial symbionts with a disproportionately large influence on the dynamics and stability of the assemblage as a whole. Second, to increase our understanding of the underlying ecological and evolutionary processes that determine the structure and dynamics of core microbiomes, which ultimately influence the functional relationship between symbionts and hosts. In my thesis, I use marine sponges and their associated bacteria as a study system. Marine sponges are one of the invertebrate phyla harbouring the largest abundance and diversity of microbes, and it is the phylogenetically oldest, still extant metazoan phyla with the hypothesized oldest microbe-host symbiotic interactions. I show that sponge-associated microbial communities emerge as one of the most specialised, yet highly diverse ecological networks ever analysed. I show that hosts harbour a core microbiome not only common to most individuals of the same species, but that cores often consist of abundant, temporally stable microbes that persistently associate to hosts over periods of years and probably even longer, and that some hosts preserve subsets of their specialised interactions by vertically transmitting microbes to the next generation. I find that the presence of high-density core microbiomes confers hosts a resistance against the increase in abundance of the many occasional microbes that pass through the sponge due to its filter-feeding activities. I show that intraspecific interactions through density-dependent dynamics together with weak interspecific interactions are likely key determinants of microbiome stability and fingerprints of coevolved interactions.
publishDate 2016
dc.date.none.fl_str_mv 2016
2016-06-03
2016
2016-11-09
dc.type.none.fl_str_mv doctoral thesis
http://purl.org/coar/resource_type/c_db06
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/doctoralThesis
format doctoralThesis
dc.identifier.none.fl_str_mv https://hdl.handle.net/2117/96369
https://dx.doi.org/10.5821/dissertation-2117-96369
url https://hdl.handle.net/2117/96369
https://dx.doi.org/10.5821/dissertation-2117-96369
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Universitat Politècnica de Catalunya
publisher.none.fl_str_mv Universitat Politècnica de Catalunya
dc.source.none.fl_str_mv reponame:UPCommons. Portal del coneixement obert de la UPC
instname:Universitat Politècnica de Catalunya (UPC)
instname_str Universitat Politècnica de Catalunya (UPC)
reponame_str UPCommons. Portal del coneixement obert de la UPC
collection UPCommons. Portal del coneixement obert de la UPC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling The structure and dynamics of complex microbe-host interaction networksBjörk, JohannesMicrobiologiaMicroorganismesÀrees temàtiques de la UPC::Enginyeria civilMicrobes form intricate and intimate relationships with most animals and plants, many of which are crucial for host development, health and functioning. Microbe--host symbiotic associations are poorly explored in comparison with other species interaction networks. The current paradigm on symbiosis research stems from species-poor systems where pairwise and reciprocally specialised interactions between a single microbe and host that coevolve are the norm. These symbioses involving just a few species are fascinating in their own right, but more diverse and complex host-associated microbial communities, so-called microbiomes, are increasingly found, with new emerging questions that require new paradigms and approaches. In this thesis, I investigate the structure and dynamics of complex microbe-host systems, focusing on the specialisation of their ecological interactions and on identifying fingerprints of coevolution in multispecies communities. I take a holistic approach to study interactions between complex assemblages of microbes associated to multiple host species through time and space. My overreaching objective is twofold. First, to determine the structure and dynamics of host-associated cores--a set of highly specialised and complementary microbial symbionts with a disproportionately large influence on the dynamics and stability of the assemblage as a whole. Second, to increase our understanding of the underlying ecological and evolutionary processes that determine the structure and dynamics of core microbiomes, which ultimately influence the functional relationship between symbionts and hosts. In my thesis, I use marine sponges and their associated bacteria as a study system. Marine sponges are one of the invertebrate phyla harbouring the largest abundance and diversity of microbes, and it is the phylogenetically oldest, still extant metazoan phyla with the hypothesized oldest microbe-host symbiotic interactions. I show that sponge-associated microbial communities emerge as one of the most specialised, yet highly diverse ecological networks ever analysed. I show that hosts harbour a core microbiome not only common to most individuals of the same species, but that cores often consist of abundant, temporally stable microbes that persistently associate to hosts over periods of years and probably even longer, and that some hosts preserve subsets of their specialised interactions by vertically transmitting microbes to the next generation. I find that the presence of high-density core microbiomes confers hosts a resistance against the increase in abundance of the many occasional microbes that pass through the sponge due to its filter-feeding activities. I show that intraspecific interactions through density-dependent dynamics together with weak interspecific interactions are likely key determinants of microbiome stability and fingerprints of coevolved interactions.Los microorganismos establecen relaciones complejas e íntimas con múltiples especies animales y vegetales, muchas de las cuales son necesarias para el desarrollo, salud y funcionamiento de sus hospedadores. Los estudios acerca de estas asociaciones simbióticas entre microbios y sus hospedadores son escasos en comparación con las investigaciones realizadas en otro tipo de redes de interacción entre especies. El paradigma actual dentro de la investigación en simbiosis proviene de sistemas con escasa diversidad biológica, donde las interacciones de especialización recíproca entre una especie de microbio y un hospedador que coevolucionan son la norma. Estas simbiosis que comprenden un escaso número de especies interaccionando entre si son fascinantes por si solas, pero se están descubriendo cada vez más comunidades microbianas mucho más diversas y complejas asociadas a otros hospedadores, conocidas como microbiomas, lo que está haciendo aparecer nuevas preguntas que requieren nuevos paradigmas y aproximaciones. En esta tesis, investigo la estructura y la dinámica de sistemas complejos de interacción entre hospedadores y microbios, centrándome en la especialización de estas interacciones ecológicas, así como en la identificación de huellas de la coevolución en comunidades con gran diversidad biológica. Adopto una perspectiva holística sobre el estudio de las interacciones entre ensamblajes complejos de microorganismos asociados a varias especies hospedadoras a lo largo del tiempo y del espacio. Tengo un doble objetivo global. En primer lugar, determinar la estructura y dinámica de los núcleos de microbios asociados a los hospedadores- definidos como aquel grupo de microbios simbiontes altamente especializados y complementarios entre si que tienen una influencia desproporcionada sobre la dinámica y estabilidad de todo el ensamblaje microbiano. En segundo lugar, mejorar nuestro conocimiento acerca de los procesos ecológicos y evolutivos responsables de la estructura y dinámica de estos núcleos del microbioma, lo que en última instancia determina las relaciones funcionales entre los simbiontes y sus hospedadores. En mi tesis utilizo las esponjas marinas y sus bacterias asociadas como sistema de estudio. Las esponjas marinas constituyen el phylum de invertebrados que albergan la mayor diversidad y abundancia de microorganismos, y es el más antiguo pero aun existente phylum, al que pertenecen las más antiguas relaciones simbiontes entre microbios y hospedadores del árbol de la vida. En mi tesis muestro que las comunidades microbianas asociadas a esponjas son una de las más especializadas, y sin embargo diversas redes ecológicas jamás mostradas. Muestro que las esponjas contienen un núcleo de microbioma que no es sólo compartido entre individuos de la misma especie, sino que además estos núcleos están formados por microbios muy abundantes que son estables a lo largo del tiempo, de modo que estos microbios permanecen asociados a sus hospedadores durante años y seguramente periodos de tiempo mucho más extensos, y distintos hospedadores conservan un grupo de estos microbios altamente especializados gracias a la transmisión vertical de los mismos a sus descendientes. Igualmente, demuestro que la presencia de núcleos del microbioma que tienen una gran densidad de simbiontes confieren una gran resistencia a sus hospedadores frente al aumento en abundancia de los muchos microbios ocasionales presentes en las esponjas debido a sus actividades de filtrado de agua de mar. Muestro también que las interacciones entre individuos de una misma especies de microorganismo, a través de la regulación denso-dependiente, junto a las interacciones de naturaleza débil entre distintas especies de microbios, son clave para entender la estabilidad y persistencia de los microbiomas y huellas inequívocas de interacciones que han coevolucionado.Universitat Politècnica de CatalunyaMontoya Terán, José M.20162016-06-0320162016-11-09doctoral thesishttp://purl.org/coar/resource_type/c_db06VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/doctoralThesisapplication/pdfhttps://hdl.handle.net/2117/96369https://dx.doi.org/10.5821/dissertation-2117-96369reponame:UPCommons. Portal del coneixement obert de la UPCinstname:Universitat Politècnica de Catalunya (UPC)Inglésengopen accesshttp://purl.org/coar/access_right/c_abf2info:eu-repo/semantics/openAccessoai:upcommons.upc.edu:2117/963692026-05-27T15:37:01Z
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