Cross-kingdom genomic variation in chicken gut microbiomes: insights from China’s diverse local breeds

TL;DR

This study explores genetic diversity in chicken gut microbiomes from China, revealing how bacteria and viruses evolve together and exchange genes.

Contribution

The study provides new insights into cross-kingdom genomic variation and horizontal gene transfer in chicken gut microbiomes using metagenomic and metatranscriptomic data.

Findings

DNA viruses showed the highest prevalence of genetic variants, with temperate phages accumulating more variants than virulent ones.

Horizontal gene transfer was strongly associated with viruses, with phage-to-bacteria transfer being a significant portion of all events.

Genomic GC content in viruses was negatively correlated with SNV density in both DNA and RNA viruses.

Abstract

The gut microbiome possesses substantial genetic diversity that supports microbial adaptation, but the genomic variation patterns across its prokaryotic and viral populations remain incompletely characterized.

Through integrated metagenomic and metatranscriptomic analysis of ten indigenous chicken breeds from China, we recovered 1527 representative prokaryotic MAGs, 37,555 representative DNA viral contigs, and 1867 representative RNA viral contigs (primarily comprising Bacillota/Bacteroidota, Uroviricota, and Lenarviricota/Pisuviricota, respectively). By integrating complementary short-read and long-read metagenomics with metatranscriptomics, we identified structural variants (SVs) and single-nucleotide variants (SNVs) in these cross-kingdom genomes. Positive SV-SNV density correlations occurred consistently across all microbial groups, indicating coordinated mutational processes. DNA viruses exhibited the highest variant prevalence (86.9% SNVs, 47.7% SVs), with temperate phages accumulating significantly more variants than virulent phages. Functionally, prokaryotic variants accumulated in carbohydrate metabolism and amino acid metabolism, while viral variants demonstrated broad metabolic hijacking. Horizontal gene transfer (HGT) was characterized by a strong virus-associated signature (69.40% of 536 events) and marked by an asymmetric pattern, with phage-to-bacteria (P-to-B) flow alone constituting 37.50% of all events. Random forest analysis revealed a strong bidirectional predictive relationship between SV and SNV densities across prokaryotic, DNA viral, and RNA viral populations, suggesting coupled genomic instability. Niche breadth emerged as a major driver of SNVs across kingdoms and was positively correlated with variant density. In prokaryotes, HGT events significantly shaped variant patterns. For viruses, genomic GC content was an important factor and consistently showed a negative correlation with SNV density in both DNA and RNA viruses.

These findings demonstrate that coordinated mutational processes and kingdom-specific intrinsic factors drive genomic variation, with viruses serving as key genetic exchange vectors in chicken gut ecosystems.

Video Abstract

Video Abstract

The online version contains supplementary material available at 10.1186/s40168-026-02347-3.

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