Impacts of Dietary Protein and Niacin Deficiency on Reproduction Performance, Body Growth, and Gut Microbiota of Female Hamsters (Tscherskia triton) and Their Offspring

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Reviewed Marked as Reviewed by Svetlana up on 2024-6-26

study design

laboratory experiment

Citation

PMID PubMed identifier for scientific articles.

36318010

DOI Digital object identifier for electronic documents.

https://doi.org/10.1128/spectrum.00157-22

URI

https://journals.asm.org/doi/10.1128/spectrum.00157-22

Authors

Zhao J, Lu W, Huang S, Le Maho Y, Habold C, Zhang Z

Journal

Microbiology spectrum

Year

2022

Keywords:

cropland monoculture, greater long-tailed hamster, gut microbiota, low-protein diet, niacin deficiency

Food resources are vital for animals to survive, and gut microbiota play an essential role in transferring nutritional materials into functional metabolites for hosts. Although the fact that diet affects host microbiota is well known, its impacts on offspring remain unclear. In this study, we assessed the effects of low-protein and niacin-deficient diets on reproduction performance, body growth, and gut microbiota of greater long-tailed hamsters (Tscherskia triton) under laboratory conditions. We found that maternal low-protein diet (not niacin deficiency) had a significant negative effect on reproduction performance of female hamsters (longer mating latency with males and smaller litter size) and body growth (lower body weight) of both female hamsters and their offspring. Both protein- and niacin-deficient diets showed significant maternal effects on the microbial community in the offspring. A maternal low-protein diet (not niacin deficiency) significantly reduced the abundance of major bacterial taxa producing short-chain fatty acids, increased the abundance of probiotic taxa, and altered microbial function in the offspring. The negative effects of maternal nutritional deficiency on gut microbiota are more pronounced in the protein group than the niacin group and in offspring more than in female hamsters. Our results suggest that a low-protein diet could alter gut microbiota in animals, which may result in negative impacts on their fitness. It is necessary to conduct further analysis to reveal the roles of nutrition, as well as its interaction with gut microbes, in affecting fitness of greater long-tailed hamsters under field conditions. IMPORTANCE Gut microbes are known to be essential for hosts to digest food and absorb nutrients. Currently, it is still unclear how maternal nutrient deficiency affects the fitness of animals by its effect on gut microbes. Here, we evaluated the effects of protein- and niacin-deficient diets on mating behavior, reproduction, body growth, and gut microbiota of both mothers and offspring of the greater long-tailed hamster (Tscherskia triton) under laboratory conditions. We found that a low-protein diet significantly reduced maternal reproduction performance and body growth of both mothers and their offspring. Both protein and niacin deficiencies showed significant maternal effects on the microbial community of the offspring. Our results hint that nutritional deficiency may be a potential factor in causing the observed sustained population decline of the greater long-tailed hamsters due to intensified monoculture in the North China Plain, and this needs further field investigation.

Experiment 1

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-8

Curated date: 2024/03/24

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Victoria, Scholastica

Subjects

Location of subjects

China

Host species Species from which microbiome was sampled. Contact us to have more species added.

Tscherskia triton

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology

Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces,feces

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology

Response to diet Response to diet,response to diet

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Female hamsters Normal-protein diet (NPD) group

Group 1 name Corresponds to the case (exposed) group for case-control studies

Female hamsters Low-protein diet (LPD) group

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Female hamsters under low-protein diet LPD

Lab analysis

Sequencing type

16S

16S variable region One or more hypervariable region(s) of the bacterial 16S gene

V3-V4

Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance

Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).

centered log-ratio

Statistical test

ANCOM

Significance threshold p-value or FDR threshold used for differential abundance testing (if any)

0.05

MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?

Yes

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-8

Curated date: 2024/03/24

Curator: Aleru Divine

Revision editor(s): Aleru Divine, KateRasheed

Source: Table S5 and Figure 5A

Description: Significant differential abundance in fecal microbiota of female hamster in Normal-protein diet (NPD) versus low-protein diet (LPD).

Abundance in Group 1: increased abundance in Female hamsters Low-protein diet (LPD) group

NCBI	Quality Control	Links
Allobaculum
Bacteroides
unclassified Bacillaceae
unclassified Veillonellaceae
Dysgonomonas
YRC22YRC22
Georgfuchsia
unclassified Prevotellaceae
Anaeroplasma
unclassified Fusobacteriaceae

Revision editor(s): Aleru Divine, KateRasheed

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-8

Curated date: 2024/03/24

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Table S5 and Figure 5A

Description: Significant differential abundance in fecal microbiota of female hamster in Normal-protein diet (NPD) versus low-protein diet (LPD).

Abundance in Group 1: decreased abundance in Female hamsters Low-protein diet (LPD) group

NCBI	Quality Control	Links
Acinetobacter
Allobaculum
Corynebacterium afermentans
Elizabethkingia
Gemmiger
Macellibacteroides
Millisia
Mucispirillum
Mycoplasma
Oleomonas
Oscillospira
Spirochaeta
unclassified Bacillota
unclassified Bacteroidota
unclassified Gammaproteobacteria
unclassified Paraprevotella
unclassified Peptostreptococcaceae
unclassified Weeksellaceae

Revision editor(s): Aleru Divine

Experiment 3

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Reviewed Marked as Reviewed by Svetlana up on 2024-6-26

Curated date: 2024/03/24

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Victoria, Scholastica

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Offspring hamsters Normal-protein diet (NPD) group

Group 1 name Corresponds to the case (exposed) group for case-control studies

Offspring hamsters Low-protein diet (LPD) group

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Offspring hamsters under low-protein diet LPD

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Richness Number of species

decreased

Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample

unchanged

Signature 1

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Reviewed Marked as Reviewed by Svetlana up on 2024-6-26

Curated date: 2024/03/24

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Table S6 and Figure 5C

Description: Significant differential abundance in fecal microbiota of offspring hamster in Normal-protein diet (NPD) versus low-protein diet (LPD).

Abundance in Group 1: increased abundance in Offspring hamsters Low-protein diet (LPD) group

NCBI	Quality Control	Links
Alkanindiges
Anaeroplasma
Arthrobacter
Bifidobacterium
Bordetella
Christensenella
Clostridium
Elizabethkingia
Lactobacillus
Millisia
Mucispirillum
Nitrobacteria
Olsenella
Pseudomonas
Pseudoxanthomonas
unclassified Actinomycetales
unclassified Comamonadaceae
unclassified Coriobacteriaceae
unclassified Lactobacillaceae
unclassified Muribaculaceae
unclassified Paraprevotella
unclassified Peptostreptococcaceae
unclassified Rikenellaceae
Unclassified YS2Unclassified YS2

Revision editor(s): Aleru Divine

Signature 2

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Curated date: 2024/03/24

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Table S6 and Figure 5C

Description: Significant differential abundance in fecal microbiota of offspring hamster in Normal-protein diet (NPD) versus low-protein diet (LPD).

Abundance in Group 1: decreased abundance in Offspring hamsters Low-protein diet (LPD) group

NCBI	Quality Control	Links
Butyricicoccus
Dorea
Gemmiger
Lachnospira
Proteiniborus
Ruminococcus
Sporobacter
unclassified Bacillota
unclassified Lachnospiraceae
Desulfovibrio
Helicobacter
unclassified Helicobacteraceae
unclassified Pseudomonadota
Brachyspira
Spirochaeta
Treponema

Revision editor(s): Aleru Divine

Experiment 4

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Reviewed Marked as Reviewed by Svetlana up on 2024-6-26

Curated date: 2024/03/24

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Victoria

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Offspring hamsters naicin+ group

Group 1 name Corresponds to the case (exposed) group for case-control studies

Offspring hamsters niacin- group

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Offspring hamsters under niacin-deficient (niacin-) diet.

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

increased

Chao1 Abundance-based estimator of species richness

increased

Richness Number of species

increased

Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample

unchanged

Signature 1

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Reviewed Marked as Reviewed by Svetlana up on 2024-6-26

Curated date: 2024/03/24

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Table S7 and Figure 5B

Description: Significant differential abundance in fecal microbiota of offspring hamster in niacin-supplemented diet (Niacin+) versus niacin-deficient diet (Niacin−).

Abundance in Group 1: increased abundance in Offspring hamsters niacin- group

NCBI	Quality Control	Links
unclassified Actinomycetales
Spirochaeta
Proteiniborus

Revision editor(s): Aleru Divine

Signature 2

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Reviewed Marked as Reviewed by Svetlana up on 2024-6-26

Curated date: 2024/03/24

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Table S7 and Figure 5B

Description: Significant differential abundance in fecal microbiota of offspring hamster in niacin-supplemented diet (Niacin+) versus niacin-deficient diet (Niacin−).

Abundance in Group 1: decreased abundance in Offspring hamsters niacin- group

NCBI	Quality Control	Links
Alkanindiges
Arthrobacter
Hespellia
Macrococcus
Mucispirillum
unclassified Comamonadaceae
unclassified Paraprevotella
unclassified Porphyromonadaceae
Clostridium

Revision editor(s): Aleru Divine