Background <p>The primary symbiont <i>Candidatus</i> Portiera is essential for nutrient provisioning in whiteflies. Genomic instability is a hallmark of <i>Bemisia tabaci</i>-associated <i>Portiera</i>, but the specific molecular evolutions and their metabolic consequences compared to <i>Portiera</i> from other whiteflies remain unclear.</p> Results <p>To overcome the limited sampling of previous studies, we assembled novel <i>Portiera</i> genomes from seven additional <i>B. tabaci</i> cryptic species. Comparative genomic, phylogenetic, and species delimitation analyses were conducted with other publicly available <i>Portiera</i> genomes. Branch-model selection analysis identified differentially evolved genes in the <i>B. tabaci</i>-associated <i>Portiera</i>, which were significantly enriched in amino acid biosynthetic pathways. The composition of essential amino acids biosynthetic pathways was systematically analyzed across <i>Portiera</i>, host nuclear, and secondary symbiont genomes. <i>B. tabaci</i>-associated <i>Portiera</i> formed a monophyletic lineage with larger genomes, lower coding density, and accelerated evolutionary rates, classified as a single species distinct from <i>Portiera</i> in other whiteflies. Twenty-two genes showed significantly different evolutionary rates with enrichment in amino acid biosynthetic pathways. Key genes for lysine and arginine biosynthesis were lost or pseudogenized in <i>B. tabaci</i>-associated <i>Portiera</i> but remained intact in other whiteflies like <i>Trialeurodes vaporariorum</i>. The synthesis of most other essential amino acids was similarly incomplete across all <i>Portiera</i>, relying on host or secondary symbiont genes for pathway completion.</p> Conclusions <p>The <i>B. tabaci</i>-associated <i>Portiera</i> represents a unique symbiotic metabolic architecture where host horizontally transferred genes may potentially compensate for <i>Portiera</i>’s genomic erosion, contrasting with the more autonomous <i>Portiera</i> in other whiteflies. This study reveals divergent evolutionary trajectories and metabolic integration strategies in whitefly symbiotic systems.</p>

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Genomic and metabolic divergence of the primary symbiont Candidatus Portiera between Bemisia tabaci and other whitefly species

  • Teng Lei,
  • Yong-Jing Fan,
  • Hong-Da Song,
  • Xin-Jia Zhang,
  • Hua-Ling Wang,
  • Chao Song,
  • Yin-Quan Liu,
  • Xin Qi

摘要

Background

The primary symbiont Candidatus Portiera is essential for nutrient provisioning in whiteflies. Genomic instability is a hallmark of Bemisia tabaci-associated Portiera, but the specific molecular evolutions and their metabolic consequences compared to Portiera from other whiteflies remain unclear.

Results

To overcome the limited sampling of previous studies, we assembled novel Portiera genomes from seven additional B. tabaci cryptic species. Comparative genomic, phylogenetic, and species delimitation analyses were conducted with other publicly available Portiera genomes. Branch-model selection analysis identified differentially evolved genes in the B. tabaci-associated Portiera, which were significantly enriched in amino acid biosynthetic pathways. The composition of essential amino acids biosynthetic pathways was systematically analyzed across Portiera, host nuclear, and secondary symbiont genomes. B. tabaci-associated Portiera formed a monophyletic lineage with larger genomes, lower coding density, and accelerated evolutionary rates, classified as a single species distinct from Portiera in other whiteflies. Twenty-two genes showed significantly different evolutionary rates with enrichment in amino acid biosynthetic pathways. Key genes for lysine and arginine biosynthesis were lost or pseudogenized in B. tabaci-associated Portiera but remained intact in other whiteflies like Trialeurodes vaporariorum. The synthesis of most other essential amino acids was similarly incomplete across all Portiera, relying on host or secondary symbiont genes for pathway completion.

Conclusions

The B. tabaci-associated Portiera represents a unique symbiotic metabolic architecture where host horizontally transferred genes may potentially compensate for Portiera’s genomic erosion, contrasting with the more autonomous Portiera in other whiteflies. This study reveals divergent evolutionary trajectories and metabolic integration strategies in whitefly symbiotic systems.