Background <p><i>Bemisia afer</i> is a globally distributed whitefly species and a significant agricultural pest, yet the genomic and functional roles of its obligate endosymbiont remain poorly understood. The primary endosymbiont of whiteflies belongs to the genus <i>Candidatus</i> Portiera. <i>Portiera</i> is essential for host survival, providing nutritional supplementation and facilitating ecological adaptation, but its evolutionary dynamics and host-specific adaptations in <i>B. afer</i> are largely unexplored. Comparative genomic studies of <i>Portiera</i> from other whitefly species have revealed distinct evolutionary patterns, yet no such data exist for <i>B. afer</i>, highlighting a critical knowledge gap.</p> Results <p>We present the first complete genome of <i>Portiera</i> BeAf, the obligate endosymbiont of <i>B. afer</i>. The genome exhibits classic signatures of reductive evolution, including extreme AT bias (25.3% GC content), high coding density (74.7%), and significant gene loss, particularly in DNA replication and repair pathway and lysine biosynthesis pathway. Average Nucleotide Identity values below the species threshold of 95% between <i>Portiera</i> BeAf and known symbionts support its designation as a novel species. Phylogenetic analyses place <i>Portiera</i> BeAf within a clade sister to <i>B. tabaci</i>-associated symbionts, yet reveal unique structural rearrangements and lineage-specific gene losses. Notably, <i>Portiera</i> BeAf harbors specific hypothetical proteins, including a putative ABCD4-like transporter, suggesting potential adaptations in nutrient transport or stress response. Comparative genomics further demonstrate weakened codon usage bias and accelerated substitution rates in <i>Bemisia</i>-associated <i>Portiera</i>, reflecting relaxed selection in their obligate symbiotic niche.</p> Conclusions <p>Our study provides foundational insights into the genomic architecture and evolutionary trajectory of <i>Portiera</i> in <i>B. afer</i>, revealing both conserved and divergent features compared to other whitefly symbionts. The loss of key metabolic and repair genes underscores the role of host compensation in maintaining symbiont functionality, while lineage-specific innovations may reflect adaptations to host ecological demands. These findings advance our understanding of <i>Portiera</i>'s genomic diversity and highlight the complex interplay between reductive evolution and host-symbiont coadaptation in ancient symbiotic systems.</p>

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The reduced genome of Candidatus Portiera sp. in Bemisia afer: evolutionary trajectories and functional implications

  • Yu-Yi Wang,
  • Yi-Jia Chen,
  • Hua-Ling Wang,
  • Cheng-Cheng Zhu,
  • Teng Lei,
  • Yin-Quan Liu

摘要

Background

Bemisia afer is a globally distributed whitefly species and a significant agricultural pest, yet the genomic and functional roles of its obligate endosymbiont remain poorly understood. The primary endosymbiont of whiteflies belongs to the genus Candidatus Portiera. Portiera is essential for host survival, providing nutritional supplementation and facilitating ecological adaptation, but its evolutionary dynamics and host-specific adaptations in B. afer are largely unexplored. Comparative genomic studies of Portiera from other whitefly species have revealed distinct evolutionary patterns, yet no such data exist for B. afer, highlighting a critical knowledge gap.

Results

We present the first complete genome of Portiera BeAf, the obligate endosymbiont of B. afer. The genome exhibits classic signatures of reductive evolution, including extreme AT bias (25.3% GC content), high coding density (74.7%), and significant gene loss, particularly in DNA replication and repair pathway and lysine biosynthesis pathway. Average Nucleotide Identity values below the species threshold of 95% between Portiera BeAf and known symbionts support its designation as a novel species. Phylogenetic analyses place Portiera BeAf within a clade sister to B. tabaci-associated symbionts, yet reveal unique structural rearrangements and lineage-specific gene losses. Notably, Portiera BeAf harbors specific hypothetical proteins, including a putative ABCD4-like transporter, suggesting potential adaptations in nutrient transport or stress response. Comparative genomics further demonstrate weakened codon usage bias and accelerated substitution rates in Bemisia-associated Portiera, reflecting relaxed selection in their obligate symbiotic niche.

Conclusions

Our study provides foundational insights into the genomic architecture and evolutionary trajectory of Portiera in B. afer, revealing both conserved and divergent features compared to other whitefly symbionts. The loss of key metabolic and repair genes underscores the role of host compensation in maintaining symbiont functionality, while lineage-specific innovations may reflect adaptations to host ecological demands. These findings advance our understanding of Portiera's genomic diversity and highlight the complex interplay between reductive evolution and host-symbiont coadaptation in ancient symbiotic systems.