Unraveling Assemblage, Functions and Stability of the Gut Microbiota of Blattella germanica by Antibiotic Treatment
Symbiosis between prokaryotes and eukaryotes is a widespread phenomenon that has contributed to the evolution of eukaryotes. In cockroaches, two types of symbionts coexist: an endosymbiont in the fat body ( ), and a rich gut microbiota. The transmission mode of is vertical, while the gut microbiota...
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| Published in | Frontiers in microbiology Vol. 11; p. 487 |
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| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
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Frontiers Media S.A
25.03.2020
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| Abstract | Symbiosis between prokaryotes and eukaryotes is a widespread phenomenon that has contributed to the evolution of eukaryotes. In cockroaches, two types of symbionts coexist: an endosymbiont in the fat body (
), and a rich gut microbiota. The transmission mode of
is vertical, while the gut microbiota of a new generation is mainly formed by bacterial species present in feces. We have carried out a metagenomic analysis of
populations, treated and non-treated with two antibiotics (vancomycin and ampicillin) over two generations to (1) determine the core of bacterial communities and potential functions of the gut microbiota and (2) to gain insights into the mechanisms of resistance and resilience of the gut microbiota. Our results indicate that the composition and functions of the bacteria were affected by treatment, more severely in the case of vancomycin. Further results demonstrated that in an untreated second-generation population that comes from antibiotic-treated first-generation, the microbiota is not yet stabilized at nymphal stages but can fully recover in adults when feces of a control population were added to the diet. This signifies the existence of a stable core in either composition and functions in lab-reared populations. The high microbiota diversity as well as the observed functional redundancy point toward the microbiota of cockroach hindguts as a robust ecosystem that can recover from perturbations, with recovery being faster when feces are added to the diet. |
|---|---|
| AbstractList | Symbiosis between prokaryotes and eukaryotes is a widespread phenomenon that has contributed to the evolution of eukaryotes. In cockroaches, two types of symbionts coexist: an endosymbiont in the fat body (Blattabacterium), and a rich gut microbiota. The transmission mode of Blattabacterium is vertical, while the gut microbiota of a new generation is mainly formed by bacterial species present in feces. We have carried out a metagenomic analysis of Blattella germanica populations, treated and non-treated with two antibiotics (vancomycin and ampicillin) over two generations to (1) determine the core of bacterial communities and potential functions of the gut microbiota and (2) to gain insights into the mechanisms of resistance and resilience of the gut microbiota. Our results indicate that the composition and functions of the bacteria were affected by treatment, more severely in the case of vancomycin. Further results demonstrated that in an untreated second-generation population that comes from antibiotic-treated first-generation, the microbiota is not yet stabilized at nymphal stages but can fully recover in adults when feces of a control population were added to the diet. This signifies the existence of a stable core in either composition and functions in lab-reared populations. The high microbiota diversity as well as the observed functional redundancy point toward the microbiota of cockroach hindguts as a robust ecosystem that can recover from perturbations, with recovery being faster when feces are added to the diet. Symbiosis between prokaryotes and eukaryotes is a widespread phenomenon that has contributed to the evolution of eukaryotes. In cockroaches, two types of symbionts coexist: an endosymbiont in the fat body ( ), and a rich gut microbiota. The transmission mode of is vertical, while the gut microbiota of a new generation is mainly formed by bacterial species present in feces. We have carried out a metagenomic analysis of populations, treated and non-treated with two antibiotics (vancomycin and ampicillin) over two generations to (1) determine the core of bacterial communities and potential functions of the gut microbiota and (2) to gain insights into the mechanisms of resistance and resilience of the gut microbiota. Our results indicate that the composition and functions of the bacteria were affected by treatment, more severely in the case of vancomycin. Further results demonstrated that in an untreated second-generation population that comes from antibiotic-treated first-generation, the microbiota is not yet stabilized at nymphal stages but can fully recover in adults when feces of a control population were added to the diet. This signifies the existence of a stable core in either composition and functions in lab-reared populations. The high microbiota diversity as well as the observed functional redundancy point toward the microbiota of cockroach hindguts as a robust ecosystem that can recover from perturbations, with recovery being faster when feces are added to the diet. Symbiosis between prokaryotes and eukaryotes is a widespread phenomenon that has contributed to the evolution of eukaryotes. In cockroaches, two types of symbionts coexist: an endosymbiont in the fat body ( Blattabacterium ), and a rich gut microbiota. The transmission mode of Blattabacterium is vertical, while the gut microbiota of a new generation is mainly formed by bacterial species present in feces. We have carried out a metagenomic analysis of Blattella germanica populations, treated and non-treated with two antibiotics (vancomycin and ampicillin) over two generations to (1) determine the core of bacterial communities and potential functions of the gut microbiota and (2) to gain insights into the mechanisms of resistance and resilience of the gut microbiota. Our results indicate that the composition and functions of the bacteria were affected by treatment, more severely in the case of vancomycin. Further results demonstrated that in an untreated second-generation population that comes from antibiotic-treated first-generation, the microbiota is not yet stabilized at nymphal stages but can fully recover in adults when feces of a control population were added to the diet. This signifies the existence of a stable core in either composition and functions in lab-reared populations. The high microbiota diversity as well as the observed functional redundancy point toward the microbiota of cockroach hindguts as a robust ecosystem that can recover from perturbations, with recovery being faster when feces are added to the diet. Symbiosis between prokaryotes and eukaryotes is a widespread phenomenon that has contributed to the evolution of eukaryotes. In cockroaches, two types of symbionts coexist: an endosymbiont in the fat body (Blattabacterium), and a rich gut microbiota. The transmission mode of Blattabacterium is vertical, while the gut microbiota of a new generation is mainly formed by bacterial species present in feces. We have carried out a metagenomic analysis of Blattella germanica populations, treated and non-treated with two antibiotics (vancomycin and ampicillin) over two generations to (1) determine the core of bacterial communities and potential functions of the gut microbiota and (2) to gain insights into the mechanisms of resistance and resilience of the gut microbiota. Our results indicate that the composition and functions of the bacteria were affected by treatment, more severely in the case of vancomycin. Further results demonstrated that in an untreated second-generation population that comes from antibiotic-treated first-generation, the microbiota is not yet stabilized at nymphal stages but can fully recover in adults when feces of a control population were added to the diet. This signifies the existence of a stable core in either composition and functions in lab-reared populations. The high microbiota diversity as well as the observed functional redundancy point toward the microbiota of cockroach hindguts as a robust ecosystem that can recover from perturbations, with recovery being faster when feces are added to the diet.Symbiosis between prokaryotes and eukaryotes is a widespread phenomenon that has contributed to the evolution of eukaryotes. In cockroaches, two types of symbionts coexist: an endosymbiont in the fat body (Blattabacterium), and a rich gut microbiota. The transmission mode of Blattabacterium is vertical, while the gut microbiota of a new generation is mainly formed by bacterial species present in feces. We have carried out a metagenomic analysis of Blattella germanica populations, treated and non-treated with two antibiotics (vancomycin and ampicillin) over two generations to (1) determine the core of bacterial communities and potential functions of the gut microbiota and (2) to gain insights into the mechanisms of resistance and resilience of the gut microbiota. Our results indicate that the composition and functions of the bacteria were affected by treatment, more severely in the case of vancomycin. Further results demonstrated that in an untreated second-generation population that comes from antibiotic-treated first-generation, the microbiota is not yet stabilized at nymphal stages but can fully recover in adults when feces of a control population were added to the diet. This signifies the existence of a stable core in either composition and functions in lab-reared populations. The high microbiota diversity as well as the observed functional redundancy point toward the microbiota of cockroach hindguts as a robust ecosystem that can recover from perturbations, with recovery being faster when feces are added to the diet. |
| Author | Domínguez-Santos, Rebeca Moya, Andrés García-Ferris, Carlos Pérez-Cobas, Ana Elena Artacho, Alejandro Latorre, Amparo Castro, José A. Talón, Irene |
| AuthorAffiliation | 2 Institut Pasteur, Biologie des Bactéries Intracellulaires , Paris , France 4 Genomics and Health Area, Foundation for the Promotion of Sanitary and Biomedical Research , Valencia , Spain 3 CNRS UMR 3525 , Paris , France 1 Institute for Integrative Systems Biology, University of Valencia and CSIC , Valencia , Spain 5 Unit of Genetics, Department of Biology, University of the Balearic Islands , Palma , Spain 6 Department of Biochemistry and Molecular Biology, University of Valencia , Valencia , Spain |
| AuthorAffiliation_xml | – name: 3 CNRS UMR 3525 , Paris , France – name: 4 Genomics and Health Area, Foundation for the Promotion of Sanitary and Biomedical Research , Valencia , Spain – name: 1 Institute for Integrative Systems Biology, University of Valencia and CSIC , Valencia , Spain – name: 6 Department of Biochemistry and Molecular Biology, University of Valencia , Valencia , Spain – name: 5 Unit of Genetics, Department of Biology, University of the Balearic Islands , Palma , Spain – name: 2 Institut Pasteur, Biologie des Bactéries Intracellulaires , Paris , France |
| Author_xml | – sequence: 1 givenname: Rebeca surname: Domínguez-Santos fullname: Domínguez-Santos, Rebeca – sequence: 2 givenname: Ana Elena surname: Pérez-Cobas fullname: Pérez-Cobas, Ana Elena – sequence: 3 givenname: Alejandro surname: Artacho fullname: Artacho, Alejandro – sequence: 4 givenname: José A. surname: Castro fullname: Castro, José A. – sequence: 5 givenname: Irene surname: Talón fullname: Talón, Irene – sequence: 6 givenname: Andrés surname: Moya fullname: Moya, Andrés – sequence: 7 givenname: Carlos surname: García-Ferris fullname: García-Ferris, Carlos – sequence: 8 givenname: Amparo surname: Latorre fullname: Latorre, Amparo |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32269557$$D View this record in MEDLINE/PubMed |
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| Cites_doi | 10.2436/20.1501.01.212 10.1038/ncomms11257 10.1002/j.1538-7305.1948.tb01338.x 10.1073/pnas.1707186114 10.1016/j.cois.2018.05.002 10.1371/journal.pone.0095476 10.1093/femsec/fiv022 10.1371/journal.ppat.1005246 10.1111/nyas.13222 10.1007/s00394-017-1445-8 10.1038/ncomms15186 10.1038/nature23292 10.1098/rsos.170003 10.1017/CBO9780511790492 10.1146/annurev-ecolsys-110617-062453 10.1146/annurev-ento-010814-020822.Multiorganismal 10.1186/1471-2105-11-119 10.1093/nar/gkn656 10.1111/mec.12874 10.3389/fmicb.2014.00335 10.1603/EN11083 10.1128/AEM.03130-15 10.1128/AEM.01837-16 10.1111/1574-6976.12025 10.4161/gmic.19896 10.1186/s12866-015-0475-8 10.1371/journal.pone.0080201 10.1371/journal.pgen.1000721 10.1016/s0167-7012(99)00033-0 10.1128/AEM.07788-11 10.1093/aesa/83.4.786 10.2147/IDR.S209591 10.1046/j.1365-294x.1998.00390.x 10.1038/nature24460 10.3390/microorganisms4010014 10.1146/annurev-micro-092412-155715 10.1128/AEM.03700-15 10.1371/journal.pone.0085861 10.1111/mec.14269 10.1016/S0022-2836(05)80360-2 10.1038/ncomms4114 10.1111/mec.14058 10.1128/AEM.70.1.293-300.2004 10.1038/nrmicro3182 10.1177/1753193411425331 10.1016/j.it.2012.05.003 10.1128/AEM.01037-18 10.1146/annurev.ento.49.061802.123416 10.1093/gbe/evu092 10.1093/bioinformatics/btr507 10.1371/journal.pone.0207985 10.1093/bioinformatics/btr026 10.1186/gb-2012-13-12-r122 10.14806/ej.17.1.200 10.1038/nature12503 10.1016/j.jhep.2013.11.034 10.1371/journal.pone.0061126 10.1128/JB.183.24.7224-7230.2001 10.1038/nmeth.1923 10.1214/aoms/1177729949 10.1093/femsec/fiy002 10.1093/nar/gkl1043 10.1038/nrmicro.2016.43 10.1007/s00248-009-9595-8 |
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| Copyright | Copyright © 2020 Domínguez-Santos, Pérez-Cobas, Artacho, Castro, Talón, Moya, García-Ferris and Latorre. Copyright © 2020 Domínguez-Santos, Pérez-Cobas, Artacho, Castro, Talón, Moya, García-Ferris and Latorre. 2020 Domínguez-Santos, Pérez-Cobas, Artacho, Castro, Talón, Moya, García-Ferris and Latorre |
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| Keywords | functional resilience Blattella germanica antibiotics endosymbiosis gut microbiota |
| Language | English |
| License | Copyright © 2020 Domínguez-Santos, Pérez-Cobas, Artacho, Castro, Talón, Moya, García-Ferris and Latorre. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by: Michael Poulsen, University of Copenhagen, Denmark Reviewed by: Alexander V. Tyakht, Institute of Gene Biology (RAS), Russia; Katie Lynn Summers, United States Department of Agriculture (USDA), United States Present address: Irene Talón, Department of Development and Regeneration, Leuven Stem Cell Institute, KU Leuven, Leuven, Belgium These authors have contributed equally to this work This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology |
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| Title | Unraveling Assemblage, Functions and Stability of the Gut Microbiota of Blattella germanica by Antibiotic Treatment |
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