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Selection against toxic aggregation-prone protein sequences in bacteria.

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  • 1Institut de Biotecnologia i de Biomedicina, Universitat Autònoma de Barcelona, E-08193 Bellaterra, Spain; Departament de Bioquímica i Biologia Molecular, Facultat de Biociències, Universitat Autònoma de Barcelona, E-08193 Bellaterra, Spain.

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Toxic protein aggregation, like that seen in Alzheimer's disease, is purged by natural selection. Bacteria experiments show that aggregation rates, not just solubility, impact cell fitness and evolution.

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Area of Science:

  • Molecular Biology
  • Evolutionary Biology
  • Biophysics

Background:

  • Genetic variation can create new protein functions, but mutations often destabilize proteins.
  • Misfolded proteins aggregate, forming cytotoxic intracellular inclusions that reduce cell fitness and cause human degenerative diseases.
  • Selection against protein misfolding and aggregation is hypothesized to constrain protein sequence evolution, but experimental validation is challenging.

Purpose of the Study:

  • To experimentally investigate the role of toxic protein aggregation in constraining protein sequence evolution.
  • To determine the relationship between in vivo aggregation propensity, aggregation rates, and cellular fitness.
  • To explore potential mechanisms for buffering the negative effects of protein aggregation.

Main Methods:

  • Utilized bacteria as a model organism to study protein aggregation and its evolutionary consequences.
  • Employed variants of the Alzheimer's-related Aβ42 peptide with differing in vivo aggregation propensities.
  • Conducted cell competition experiments and flow cytometry analysis to assess cellular metabolism, viability, and aggregation burden.

Main Results:

  • Aggregation-prone Aβ42 variants were eliminated from growing bacterial populations, indicating strong purifying selection.
  • A clear correlation was observed between physiological burden, aggregation propensity, and the purifying effect.
  • The fitness cost of aggregation was linked to aggregation rates rather than overall protein solubility.
  • The osmolyte proline mitigated the metabolic impact of protein aggregation by reducing in vivo aggregation rates.

Conclusions:

  • Toxic protein aggregation significantly impacts the cell fitness landscape.
  • Aggregation rates, not just solubility, are a key factor in the selective pressure against misfolded proteins.
  • These findings provide experimental evidence supporting the role of protein aggregation in shaping the evolution of natural protein sequences.