The Native Microbiome is Crucial for Offspring Generation and Fitness of <italic toggle="yes">Aurelia aurita</italic>
ABSTRACT All multicellular organisms are associated with microbial communities, ultimately forming a metaorganism. Several studies conducted on well-established model organisms point to immunological, metabolic, and behavioral benefits of the associated microbiota for the host. Consequently, a micro...
Guardado en:
| Autores principales: | , , , , , , , |
|---|---|
| Formato: | article |
| Lenguaje: | EN |
| Publicado: |
American Society for Microbiology
2020
|
| Materias: | |
| Acceso en línea: | https://doaj.org/article/e1f8f18b70874b199711ea3a480518b0 |
| Etiquetas: |
Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
|
| id |
oai:doaj.org-article:e1f8f18b70874b199711ea3a480518b0 |
|---|---|
| record_format |
dspace |
| spelling |
oai:doaj.org-article:e1f8f18b70874b199711ea3a480518b02021-11-15T15:55:43ZThe Native Microbiome is Crucial for Offspring Generation and Fitness of <italic toggle="yes">Aurelia aurita</italic>10.1128/mBio.02336-202150-7511https://doaj.org/article/e1f8f18b70874b199711ea3a480518b02020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02336-20https://doaj.org/toc/2150-7511ABSTRACT All multicellular organisms are associated with microbial communities, ultimately forming a metaorganism. Several studies conducted on well-established model organisms point to immunological, metabolic, and behavioral benefits of the associated microbiota for the host. Consequently, a microbiome can influence the physiology of a host; moreover, microbial community shifts can affect host health and fitness. The present study aimed to evaluate the significance and functional role of the native microbiota for life cycle transitions and fitness of the cnidarian moon jellyfish Aurelia aurita. A comprehensive host fitness experiment was conducted studying the polyp life stage and integrating 12 combinations of treatments with microbiota modification (sterile conditions, foreign food bacteria, and potential pathogens). Asexual reproduction, e.g., generation of daughter polyps, and the formation and release of ephyrae were highly affected in the absence of the native microbiota, ultimately resulting in a halt of strobilation and ephyra release. Assessment of further fitness traits showed that health, growth, and feeding rate were decreased in the absence and upon community changes of the native microbiota, e.g., when challenged with selected bacteria. Moreover, changes in microbial community patterns were detected by 16S rRNA amplicon sequencing during the course of the experiment. This demonstrated that six operational taxonomic units (OTUs) significantly correlated and explained up to 97% of fitness data variability, strongly supporting the association of impaired fitness with the absence/presence of specific bacteria. Conclusively, our study provides new insights into the importance and function of the microbiome for asexual reproduction, health, and fitness of the basal metazoan A. aurita. IMPORTANCE All multicellular organisms are associated with a diverse and specific community of microorganisms; consequently, the microbiome is of fundamental importance for health and fitness of the multicellular host. However, studies on microbiome contribution to host fitness are in their infancy, in particular, for less well-established hosts such as the moon jellyfish Aurelia aurita. Here, we studied the impact of the native microbiome on the asexual reproduction and on further fitness traits (health, growth, and feeding) of the basal metazoan due to induced changes in its microbiome. We observed significant impact on all fitness traits analyzed, in particular, in the absence of the protective microbial shield and when challenged with marine potentially pathogenic bacterial isolates. Notable is the identified crucial importance of the native microbiome for the generation of offspring, consequently affecting life cycle decisions. Thus, we conclude that the microbiome is essential for the maintenance of a healthy metaorganism.Nancy Weiland-BräuerNicole PinnowDaniela LangfeldtAnna RoikSimon GüllertCynthia M. ChibaniThorsten B. H. ReuschRuth A. SchmitzAmerican Society for MicrobiologyarticleAurelia auritahosthost fitnessmicrobiomemicrobiotareproductionMicrobiologyQR1-502ENmBio, Vol 11, Iss 6 (2020) |
| institution |
DOAJ |
| collection |
DOAJ |
| language |
EN |
| topic |
Aurelia aurita host host fitness microbiome microbiota reproduction Microbiology QR1-502 |
| spellingShingle |
Aurelia aurita host host fitness microbiome microbiota reproduction Microbiology QR1-502 Nancy Weiland-Bräuer Nicole Pinnow Daniela Langfeldt Anna Roik Simon Güllert Cynthia M. Chibani Thorsten B. H. Reusch Ruth A. Schmitz The Native Microbiome is Crucial for Offspring Generation and Fitness of <italic toggle="yes">Aurelia aurita</italic> |
| description |
ABSTRACT All multicellular organisms are associated with microbial communities, ultimately forming a metaorganism. Several studies conducted on well-established model organisms point to immunological, metabolic, and behavioral benefits of the associated microbiota for the host. Consequently, a microbiome can influence the physiology of a host; moreover, microbial community shifts can affect host health and fitness. The present study aimed to evaluate the significance and functional role of the native microbiota for life cycle transitions and fitness of the cnidarian moon jellyfish Aurelia aurita. A comprehensive host fitness experiment was conducted studying the polyp life stage and integrating 12 combinations of treatments with microbiota modification (sterile conditions, foreign food bacteria, and potential pathogens). Asexual reproduction, e.g., generation of daughter polyps, and the formation and release of ephyrae were highly affected in the absence of the native microbiota, ultimately resulting in a halt of strobilation and ephyra release. Assessment of further fitness traits showed that health, growth, and feeding rate were decreased in the absence and upon community changes of the native microbiota, e.g., when challenged with selected bacteria. Moreover, changes in microbial community patterns were detected by 16S rRNA amplicon sequencing during the course of the experiment. This demonstrated that six operational taxonomic units (OTUs) significantly correlated and explained up to 97% of fitness data variability, strongly supporting the association of impaired fitness with the absence/presence of specific bacteria. Conclusively, our study provides new insights into the importance and function of the microbiome for asexual reproduction, health, and fitness of the basal metazoan A. aurita. IMPORTANCE All multicellular organisms are associated with a diverse and specific community of microorganisms; consequently, the microbiome is of fundamental importance for health and fitness of the multicellular host. However, studies on microbiome contribution to host fitness are in their infancy, in particular, for less well-established hosts such as the moon jellyfish Aurelia aurita. Here, we studied the impact of the native microbiome on the asexual reproduction and on further fitness traits (health, growth, and feeding) of the basal metazoan due to induced changes in its microbiome. We observed significant impact on all fitness traits analyzed, in particular, in the absence of the protective microbial shield and when challenged with marine potentially pathogenic bacterial isolates. Notable is the identified crucial importance of the native microbiome for the generation of offspring, consequently affecting life cycle decisions. Thus, we conclude that the microbiome is essential for the maintenance of a healthy metaorganism. |
| format |
article |
| author |
Nancy Weiland-Bräuer Nicole Pinnow Daniela Langfeldt Anna Roik Simon Güllert Cynthia M. Chibani Thorsten B. H. Reusch Ruth A. Schmitz |
| author_facet |
Nancy Weiland-Bräuer Nicole Pinnow Daniela Langfeldt Anna Roik Simon Güllert Cynthia M. Chibani Thorsten B. H. Reusch Ruth A. Schmitz |
| author_sort |
Nancy Weiland-Bräuer |
| title |
The Native Microbiome is Crucial for Offspring Generation and Fitness of <italic toggle="yes">Aurelia aurita</italic> |
| title_short |
The Native Microbiome is Crucial for Offspring Generation and Fitness of <italic toggle="yes">Aurelia aurita</italic> |
| title_full |
The Native Microbiome is Crucial for Offspring Generation and Fitness of <italic toggle="yes">Aurelia aurita</italic> |
| title_fullStr |
The Native Microbiome is Crucial for Offspring Generation and Fitness of <italic toggle="yes">Aurelia aurita</italic> |
| title_full_unstemmed |
The Native Microbiome is Crucial for Offspring Generation and Fitness of <italic toggle="yes">Aurelia aurita</italic> |
| title_sort |
native microbiome is crucial for offspring generation and fitness of <italic toggle="yes">aurelia aurita</italic> |
| publisher |
American Society for Microbiology |
| publishDate |
2020 |
| url |
https://doaj.org/article/e1f8f18b70874b199711ea3a480518b0 |
| work_keys_str_mv |
AT nancyweilandbrauer thenativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT nicolepinnow thenativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT danielalangfeldt thenativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT annaroik thenativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT simongullert thenativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT cynthiamchibani thenativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT thorstenbhreusch thenativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT ruthaschmitz thenativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT nancyweilandbrauer nativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT nicolepinnow nativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT danielalangfeldt nativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT annaroik nativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT simongullert nativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT cynthiamchibani nativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT thorstenbhreusch nativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic AT ruthaschmitz nativemicrobiomeiscrucialforoffspringgenerationandfitnessofitalictoggleyesaureliaauritaitalic |
| _version_ |
1718427185235099648 |