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Heuristic Mining of Hierarchical Genotypes and Accessory Genome Loci in Bacterial Populations

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A Population Genomics Approach to Assessing the Genetic Basis of Within-Host Microevolution Underlying Recurrent

Johanna Rhodes¹, Mathew A Beale², Mathieu Vanhove¹

¹Department of Infectious Disease Epidemiology, Imperial College London, W2 1PG United Kingdom.

G3 (Bethesda, Md.)

|February 12, 2017

Summary

Recurrent cryptococcal meningitis in HIV/AIDS patients is often relapse, not reinfection. Whole-genome sequencing revealed novel mutations causing a hypermutator state, enabling rapid evolution and antifungal drug resistance in Cryptococcus neoformans.

Keywords:

cryptococcosis evolution genomics hypermutation resistance

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Area of Science:

Mycology
Genetics
Infectious Diseases

Background:

Recurrent cryptococcal meningitis (CM) is a significant cause of mortality in HIV/AIDS patients, particularly in sub-Saharan Africa.
Distinguishing between relapse from the original infection and reinfection with a new isolate is crucial for effective treatment and management.

Purpose of the Study:

To investigate the genetic basis of recurrent CM in HIV-infected individuals.
To determine whether recurrence is due to relapse of the original Cryptococcus neoformans isolate or reinfection with a different isolate.

Main Methods:

Whole-genome sequencing (WGS) was employed to analyze paired isolates from 17 HIV-infected individuals with recurrent CM.
Genetic comparisons were made between isolates obtained before and after recurrence.

Main Results:

Fifteen out of 17 pairs of isolates showed a clonal relationship, indicating relapse of the original infection.
Two pairs exhibited high genetic heterogeneity. One was due to mixed genotype infection, and the other resulted from nonsense mutations in DNA mismatch repair genes (MSH2, MSH5, RAD5).
These mutations induced a hypermutator state in C. neoformans, increasing substitution rates and potentially facilitating rapid within-host evolution and antifungal drug resistance.

Conclusions:

Recurrence of CM in this cohort was predominantly due to relapse of the original Cryptococcus neoformans infection.
Novel nonsense mutations in DNA mismatch repair genes can lead to a hypermutator phenotype in C. neoformans.
This hypermutator state represents a new mechanism for rapid within-host adaptation and the evolution of antifungal drug resistance in C. neoformans, with significant implications for patient outcomes.