Critical complex network structures in animal gastrointestinal tract microbiomes.

Bacteroidetes/Firmicutes (BF) ratio Bacteroidetes/Proteobacteria (B/P) ratio Firmicutes/Proteobacteria (F/P) ratio Animal gastrointestinal tract microbiomes (AGM) Core/periphery network (CPN) High-salience skeleton network (HSN) Host diets and animal gut microbiomes Phylogenetic (evolutionary) timeline (PT)

Journal

Animal microbiome
ISSN: 2524-4671
Titre abrégé: Anim Microbiome
Pays: England
ID NLM: 101759457

Informations de publication

Date de publication:
03 May 2024
Historique:
received: 08 04 2023
accepted: 21 01 2024
medline: 4 5 2024
pubmed: 4 5 2024
entrez: 3 5 2024
Statut: epublish

Résumé

Living things from microbes to their hosts (plants, animals and humans) interact with each other, and their relationships may be described with complex network models. The present study focuses on the critical network structures, specifically the core/periphery nodes and backbones (paths of high-salience skeletons) in animal gastrointestinal microbiomes (AGMs) networks. The core/periphery network (CPN) mirrors nearly ubiquitous nestedness in ecological communities, particularly dividing the network as densely interconnected core-species and periphery-species that only sparsely linked to the core. Complementarily, the high-salience skeleton network (HSN) mirrors the pervasive asymmetrical species interactions (strictly microbial species correlations), particularly forming heterogenous pathways in AGM networks with both "backbones" and "rural roads" (regular or weak links). While the cores and backbones can act as critical functional structures, the periphery nodes and weak links may stabilize network functionalities through redundancy. Here, we build and analyze 36 pairs of CPN/HSN for the AGMs based on 4903 gastrointestinal-microbiome samples containing 473,359 microbial species collected from 318 animal species covering all vertebrate and four major invertebrate classes. The network analyses were performed at host species, order, class, phylum, kingdom scales and diet types with selected and comparative taxon pairs. Besides diet types, the influence of host phylogeny, measured with phylogenetic (evolutionary) timeline or "age", were integrated into the analyses. For example, it was found that the evolutionary trends of three primary microbial phyla (Bacteroidetes/Firmicutes/Proteobacteria) and their pairwise abundance-ratios in animals do not mirror the patterns in modern humans phylogenetically, although they are consistent in terms of diet types. Overall, the critical network structures of AGMs are qualitatively and structurally similar to those of the human gut microbiomes. Nevertheless, it appears that the critical composition (the three phyla of Bacteroidetes, Firmicutes, and Proteobacteria) in human gut microbiomes has broken the evolutionary trend from animals to humans, possibly attributable to the Anthropocene epoch and reflecting the far-reaching influences of agriculture and industrial revolution on the human gut microbiomes. The influences may have led to the deviations between modern humans and our hunter-gather ancestors and animals.

Sections du résumé

BACKGROUND BACKGROUND
Living things from microbes to their hosts (plants, animals and humans) interact with each other, and their relationships may be described with complex network models. The present study focuses on the critical network structures, specifically the core/periphery nodes and backbones (paths of high-salience skeletons) in animal gastrointestinal microbiomes (AGMs) networks. The core/periphery network (CPN) mirrors nearly ubiquitous nestedness in ecological communities, particularly dividing the network as densely interconnected core-species and periphery-species that only sparsely linked to the core. Complementarily, the high-salience skeleton network (HSN) mirrors the pervasive asymmetrical species interactions (strictly microbial species correlations), particularly forming heterogenous pathways in AGM networks with both "backbones" and "rural roads" (regular or weak links). While the cores and backbones can act as critical functional structures, the periphery nodes and weak links may stabilize network functionalities through redundancy.
RESULTS RESULTS
Here, we build and analyze 36 pairs of CPN/HSN for the AGMs based on 4903 gastrointestinal-microbiome samples containing 473,359 microbial species collected from 318 animal species covering all vertebrate and four major invertebrate classes. The network analyses were performed at host species, order, class, phylum, kingdom scales and diet types with selected and comparative taxon pairs. Besides diet types, the influence of host phylogeny, measured with phylogenetic (evolutionary) timeline or "age", were integrated into the analyses. For example, it was found that the evolutionary trends of three primary microbial phyla (Bacteroidetes/Firmicutes/Proteobacteria) and their pairwise abundance-ratios in animals do not mirror the patterns in modern humans phylogenetically, although they are consistent in terms of diet types.
CONCLUSIONS CONCLUSIONS
Overall, the critical network structures of AGMs are qualitatively and structurally similar to those of the human gut microbiomes. Nevertheless, it appears that the critical composition (the three phyla of Bacteroidetes, Firmicutes, and Proteobacteria) in human gut microbiomes has broken the evolutionary trend from animals to humans, possibly attributable to the Anthropocene epoch and reflecting the far-reaching influences of agriculture and industrial revolution on the human gut microbiomes. The influences may have led to the deviations between modern humans and our hunter-gather ancestors and animals.

Identifiants

pubmed: 38702785
doi: 10.1186/s42523-024-00291-x
pii: 10.1186/s42523-024-00291-x
doi:

Types de publication

Journal Article

Langues

eng

Pagination

23

Informations de copyright

© 2024. The Author(s).

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Auteurs

Zhanshan Sam Ma (ZS)

Computational Biology and Medical Ecology Lab, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China. zhanshanma@fas.harvard.edu.
Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, China. zhanshanma@fas.harvard.edu.
Faculty of Arts and Science, Harvard Forest, Harvard University, Cambridge, MA, 02138, USA. zhanshanma@fas.harvard.edu.

Peng Shi (P)

Evolutionary and Functional Genomics Lab, State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China. ship@mail.kiz.ac.cn.
Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, China. ship@mail.kiz.ac.cn.

Classifications MeSH