Adaptability of the gut microbiota of the German cockroach Blattella germanica to a periodic antibiotic treatment

High-throughput sequencing studies have shown that diet or antimicrobial treatments impact animal gut microbiota equilibrium. However, properties related to the gut microbial ecosystem stability, such as resilience, resistance, or functional redundancy, must be better understood. To shed light on th...

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Published inMicrobiological research Vol. 287; p. 127863
Main Authors Marín-Miret, Jesús, Pérez-Cobas, Ana Elena, Domínguez-Santos, Rebeca, Pérez-Rocher, Benjamí, Latorre, Amparo, Moya, Andrés
Format Journal Article
LanguageEnglish
Published Germany Elsevier GmbH 01.10.2024
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Abstract High-throughput sequencing studies have shown that diet or antimicrobial treatments impact animal gut microbiota equilibrium. However, properties related to the gut microbial ecosystem stability, such as resilience, resistance, or functional redundancy, must be better understood. To shed light on these ecological processes, we combined advanced statistical methods with 16 S rRNA gene sequencing, functional prediction, and fitness analyses in the gut microbiota of the cockroach Blattella germanica subject to three periodic pulses of the antibiotic (AB) kanamycin (n=512). We first confirmed that AB did not significantly affect cockroaches' biological fitness, and gut microbiota changes were not caused by insect physiology alterations. The sex variable was examined for the first time in this species, and no statistical differences in the gut microbiota diversity or composition were found. The comparison of the gut microbiota dynamics in control and treated populations revealed that (1) AB treatment decreases diversity and completely disrupts the co-occurrence networks between bacteria, significantly altering the gut community structure. (2) Although AB also affected the genetic composition, functional redundancy would explain a smaller effect on the functional potential than on the taxonomic composition. (3) As predicted by Taylor's law, AB generally affected the most abundant taxa to a lesser extent than the less abundant taxa. (4) Taxa follow different trends in response to ABs, highlighting "resistant taxa," which could be critical for community restoration. (5) The gut microbiota recovered faster after the three AB pulses, suggesting that gut microbiota adapts to repeated treatments. •Antibiotics do not directly affect B. germanica physiology.•Males and females of B. germanica have similar gut microbial communities.•Antibiotics disturb the network of interactions in the cockroach gut microbiome.•Gut functional redundancy buffers the effect of antibiotics.•Gut microbiota adapts to repeated antibiotic treatments.
AbstractList High-throughput sequencing studies have shown that diet or antimicrobial treatments impact animal gut microbiota equilibrium. However, properties related to the gut microbial ecosystem stability, such as resilience, resistance, or functional redundancy, must be better understood. To shed light on these ecological processes, we combined advanced statistical methods with 16 S rRNA gene sequencing, functional prediction, and fitness analyses in the gut microbiota of the cockroach Blattella germanica subject to three periodic pulses of the antibiotic (AB) kanamycin (n=512). We first confirmed that AB did not significantly affect cockroaches' biological fitness, and gut microbiota changes were not caused by insect physiology alterations. The sex variable was examined for the first time in this species, and no statistical differences in the gut microbiota diversity or composition were found. The comparison of the gut microbiota dynamics in control and treated populations revealed that (1) AB treatment decreases diversity and completely disrupts the co-occurrence networks between bacteria, significantly altering the gut community structure. (2) Although AB also affected the genetic composition, functional redundancy would explain a smaller effect on the functional potential than on the taxonomic composition. (3) As predicted by Taylor's law, AB generally affected the most abundant taxa to a lesser extent than the less abundant taxa. (4) Taxa follow different trends in response to ABs, highlighting "resistant taxa," which could be critical for community restoration. (5) The gut microbiota recovered faster after the three AB pulses, suggesting that gut microbiota adapts to repeated treatments.
High-throughput sequencing studies have shown that diet or antimicrobial treatments impact animal gut microbiota equilibrium. However, properties related to the gut microbial ecosystem stability, such as resilience, resistance, or functional redundancy, must be better understood. To shed light on these ecological processes, we combined advanced statistical methods with 16 S rRNA gene sequencing, functional prediction, and fitness analyses in the gut microbiota of the cockroach Blattella germanica subject to three periodic pulses of the antibiotic (AB) kanamycin (n=512). We first confirmed that AB did not significantly affect cockroaches' biological fitness, and gut microbiota changes were not caused by insect physiology alterations. The sex variable was examined for the first time in this species, and no statistical differences in the gut microbiota diversity or composition were found. The comparison of the gut microbiota dynamics in control and treated populations revealed that (1) AB treatment decreases diversity and completely disrupts the co-occurrence networks between bacteria, significantly altering the gut community structure. (2) Although AB also affected the genetic composition, functional redundancy would explain a smaller effect on the functional potential than on the taxonomic composition. (3) As predicted by Taylor's law, AB generally affected the most abundant taxa to a lesser extent than the less abundant taxa. (4) Taxa follow different trends in response to ABs, highlighting "resistant taxa," which could be critical for community restoration. (5) The gut microbiota recovered faster after the three AB pulses, suggesting that gut microbiota adapts to repeated treatments.High-throughput sequencing studies have shown that diet or antimicrobial treatments impact animal gut microbiota equilibrium. However, properties related to the gut microbial ecosystem stability, such as resilience, resistance, or functional redundancy, must be better understood. To shed light on these ecological processes, we combined advanced statistical methods with 16 S rRNA gene sequencing, functional prediction, and fitness analyses in the gut microbiota of the cockroach Blattella germanica subject to three periodic pulses of the antibiotic (AB) kanamycin (n=512). We first confirmed that AB did not significantly affect cockroaches' biological fitness, and gut microbiota changes were not caused by insect physiology alterations. The sex variable was examined for the first time in this species, and no statistical differences in the gut microbiota diversity or composition were found. The comparison of the gut microbiota dynamics in control and treated populations revealed that (1) AB treatment decreases diversity and completely disrupts the co-occurrence networks between bacteria, significantly altering the gut community structure. (2) Although AB also affected the genetic composition, functional redundancy would explain a smaller effect on the functional potential than on the taxonomic composition. (3) As predicted by Taylor's law, AB generally affected the most abundant taxa to a lesser extent than the less abundant taxa. (4) Taxa follow different trends in response to ABs, highlighting "resistant taxa," which could be critical for community restoration. (5) The gut microbiota recovered faster after the three AB pulses, suggesting that gut microbiota adapts to repeated treatments.
High-throughput sequencing studies have shown that diet or antimicrobial treatments impact animal gut microbiota equilibrium. However, properties related to the gut microbial ecosystem stability, such as resilience, resistance, or functional redundancy, must be better understood. To shed light on these ecological processes, we combined advanced statistical methods with 16 S rRNA gene sequencing, functional prediction, and fitness analyses in the gut microbiota of the cockroach Blattella germanica subject to three periodic pulses of the antibiotic (AB) kanamycin (n=512). We first confirmed that AB did not significantly affect cockroaches' biological fitness, and gut microbiota changes were not caused by insect physiology alterations. The sex variable was examined for the first time in this species, and no statistical differences in the gut microbiota diversity or composition were found. The comparison of the gut microbiota dynamics in control and treated populations revealed that (1) AB treatment decreases diversity and completely disrupts the co-occurrence networks between bacteria, significantly altering the gut community structure. (2) Although AB also affected the genetic composition, functional redundancy would explain a smaller effect on the functional potential than on the taxonomic composition. (3) As predicted by Taylor's law, AB generally affected the most abundant taxa to a lesser extent than the less abundant taxa. (4) Taxa follow different trends in response to ABs, highlighting "resistant taxa," which could be critical for community restoration. (5) The gut microbiota recovered faster after the three AB pulses, suggesting that gut microbiota adapts to repeated treatments. •Antibiotics do not directly affect B. germanica physiology.•Males and females of B. germanica have similar gut microbial communities.•Antibiotics disturb the network of interactions in the cockroach gut microbiome.•Gut functional redundancy buffers the effect of antibiotics.•Gut microbiota adapts to repeated antibiotic treatments.
ArticleNumber 127863
Author Domínguez-Santos, Rebeca
Pérez-Rocher, Benjamí
Moya, Andrés
Latorre, Amparo
Pérez-Cobas, Ana Elena
Marín-Miret, Jesús
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  givenname: Ana Elena
  surname: Pérez-Cobas
  fullname: Pérez-Cobas, Ana Elena
  organization: Department of Microbiology, Ramón y Cajal Institute for Health Research (IRYCIS), Ramón y Cajal University Hospital, Madrid, Spain; CIBER in Infectious Diseases (CIBERINFEC), Madrid, Spain
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  givenname: Rebeca
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  givenname: Benjamí
  surname: Pérez-Rocher
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  surname: Latorre
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  surname: Moya
  fullname: Moya, Andrés
  email: andres.moya@uv.es
  organization: Institute for Integrative Systems Biology (I2SysBio), University of Valencia and Spanish Research Council, Paterna, Valencia 46980, Spain
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Keywords Gut microbiota
Cockroach
Resistance
Antibiotic treatment
Resilience
Language English
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Snippet High-throughput sequencing studies have shown that diet or antimicrobial treatments impact animal gut microbiota equilibrium. However, properties related to...
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SubjectTerms Adaptation, Physiological
Animals
Anti-Bacterial Agents - pharmacology
Antibiotic treatment
Bacteria - classification
Bacteria - drug effects
Bacteria - genetics
Bacteria - isolation & purification
Biodiversity
Blattellidae - microbiology
Cockroach
Cockroaches - drug effects
Cockroaches - microbiology
Female
Gastrointestinal Microbiome - drug effects
Gut microbiota
High-Throughput Nucleotide Sequencing
Kanamycin - pharmacology
Male
Phylogeny
Resilience
Resistance
RNA, Ribosomal, 16S - genetics
Title Adaptability of the gut microbiota of the German cockroach Blattella germanica to a periodic antibiotic treatment
URI https://dx.doi.org/10.1016/j.micres.2024.127863
https://www.ncbi.nlm.nih.gov/pubmed/39106785
https://www.proquest.com/docview/3089879276
Volume 287
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