1. Microbiology and Infectious Disease
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Genetic basis for coordination of meiosis and sexual structure maturation in Cryptococcus neoformans

  1. Linxia Liu
  2. Guang-Jun He
  3. Lei Chen
  4. Jiao Zheng
  5. Yingying Chen
  6. Lan Shen
  7. Xiuyun Tian
  8. Erwei Li
  9. Ence Yang
  10. Guojian Liao
  11. Linqi Wang  Is a corresponding author
  1. Institute of Microbiology, Chinese Academy of Sciences, China
  2. Southwest University, China
  3. School of Basic Medical Sciences, Peking University Health Science Center, China
Research Article
  • Cited 10
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Cite this article as: eLife 2018;7:e38683 doi: 10.7554/eLife.38683

Abstract

In the human fungal pathogen Cryptococcus neoformans, sex can benefit its pathogenicity through production of meiospores, which are believed to offer both physical and meiosis-created lineage advantages for its infections. Cryptococcus sporulation occurs following two parallel events, meiosis and differentiation of the basidium, the characteristic sexual structure of the basidiomycetes. However, the circuit integrating these events to ensure subsequent sporulation is unclear. Here, we show the spatiotemporal coordination of meiosis and basidial maturation by visualizing event-specific molecules in developing basidia defined by a quantitative approach. Monitoring of gene induction timing together with genetic analysis reveals co-regulation of the coordinated events by a shared regulatory program. Two RRM family regulators, Csa1 and Csa2, are crucial components that specifically bridge meiosis and basidial maturation, further determining sporulation. We propose that the regulatory coordination of meiosis and basidial development serves as a determinant underlying the production of infectious meiospores in C. neoformans.

Data availability

The GEO accession number for the RNA-seq data reported in this study is GSE111975.

The following data sets were generated

Article and author information

Author details

  1. Linxia Liu

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Guang-Jun He

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Lei Chen

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Jiao Zheng

    College of Pharmaceutical Sciences, Southwest University, Chongqing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Yingying Chen

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Lan Shen

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Xiuyun Tian

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Erwei Li

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Ence Yang

    Department of Microbiology, School of Basic Medical Sciences, Peking University Health Science Center, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Guojian Liao

    Institute of Morden Biopharmaceuticals, School of Pharmaceutical Sciences, Southwest University, Chongqing, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Linqi Wang

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    For correspondence
    wanglq@im.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5243-341X

Funding

Ministry of Science and Technology of the People's Republic of China (2018ZX10101004)

  • Linqi Wang

National Natural Science Foundation of China (31622004,31570138,31770163)

  • Linqi Wang

Chinese Academy of Sciences Key Project (QYZDB-SSW-SSMC040)

  • Linqi Wang

National Natural Science Foundation of China (31501008)

  • Guang-Jun He

National Natural Science Foundation of China (31501009)

  • Xiuyun Tian

The funders had roles in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Joseph Heitman, Duke University, United States

Publication history

  1. Received: May 26, 2018
  2. Accepted: October 2, 2018
  3. Accepted Manuscript published: October 3, 2018 (version 1)
  4. Version of Record published: November 14, 2018 (version 2)

Copyright

© 2018, Liu et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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Further reading

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    Sofiene Seef et al.
    Research Article Updated

    Myxococcus xanthus, a soil bacterium, predates collectively using motility to invade prey colonies. Prey lysis is mostly thought to rely on secreted factors, cocktails of antibiotics and enzymes, and direct contact with Myxococcus cells. In this study, we show that on surfaces the coupling of A-motility and contact-dependent killing is the central predatory mechanism driving effective prey colony invasion and consumption. At the molecular level, contact-dependent killing involves a newly discovered type IV filament-like machinery (Kil) that both promotes motility arrest and prey cell plasmolysis. In this process, Kil proteins assemble at the predator-prey contact site, suggesting that they allow tight contact with prey cells for their intoxication. Kil-like systems form a new class of Tad-like machineries in predatory bacteria, suggesting a conserved function in predator-prey interactions. This study further reveals a novel cell-cell interaction function for bacterial pili-like assemblages.

    1. Medicine
    2. Microbiology and Infectious Disease
    Alexander O Pasternak et al.
    Research Article Updated

    Background:

    It remains unclear whether combination antiretroviral therapy (ART) regimens differ in their ability to fully suppress human immunodeficiency virus (HIV) replication. Here, we report the results of two cross-sectional studies that compared levels of cell-associated (CA) HIV markers between individuals receiving suppressive ART containing either a non-nucleoside reverse transcriptase inhibitor (NNRTI) or a protease inhibitor (PI).

    Methods:

    CA HIV unspliced RNA and total HIV DNA were quantified in two cohorts (n = 100, n = 124) of individuals treated with triple ART regimens consisting of two nucleoside reverse transcriptase inhibitors (NRTIs) plus either an NNRTI or a PI. To compare CA HIV RNA and DNA levels between the regimens, we built multivariable models adjusting for age, gender, current and nadir CD4+ count, plasma viral load zenith, duration of virological suppression, NRTI backbone composition, low-level plasma HIV RNA detectability, and electronically measured adherence to ART.

    Results:

    In both cohorts, levels of CA HIV RNA and DNA strongly correlated (rho = 0.70 and rho = 0.54) and both markers were lower in NNRTI-treated than in PI-treated individuals. In the multivariable analysis, CA RNA in both cohorts remained significantly reduced in NNRTI-treated individuals (padj = 0.02 in both cohorts), with a similar but weaker association between the ART regimen and total HIV DNA (padj = 0.048 and padj = 0.10). No differences in CA HIV RNA or DNA levels were observed between individual NNRTIs or individual PIs, but CA HIV RNA was lower in individuals treated with either nevirapine or efavirenz, compared to PI-treated individuals.

    Conclusions:

    All current classes of antiretroviral drugs only prevent infection of new cells but do not inhibit HIV RNA transcription in long-lived reservoir cells. Therefore, these differences in CA HIV RNA and DNA levels by treatment regimen suggest that NNRTIs are more potent in suppressing HIV residual replication than PIs, which may result in a smaller viral reservoir size.

    Funding:

    This work was supported by ZonMw (09120011910035) and FP7 Health (305522).