Much headway has been made in understanding the numerous strategies that enable microorganisms to counteract various types of environmental stress, but little is known about how microbial populations recover after a massive death caused by exposure to extreme conditions. Using the yeast-like fungus Ustilago maydis as a model, our recent post-stress regrowth under starvation (RUS) studies have demonstrated that this organism reconstitutes devastated populations with remarkable efficiency. Subsequently, we have identified four RUS-gene products. Two of these, Did4 and Tbp1, play parallel roles in protecting the genome. To identify additional molecular components, we took a molecular-genetic and a transcriptomic approach. By employing a simple and novel screening method, we identified five RUS-deficient mutants (snf8, slm1, vrg4, snf5, hsf1), three of which (snf8, slm1, and hsf1) displayed sensitivity to different genotoxic agents, indicating that the corresponding gene products have roles in genome protection. The global transcriptomic changes of cells grown in supernatants derived from peroxide-treated cell suspensions revealed sets of uniquely expressed genes. Importantly, among the genes induced by the substrates was Chk1, which encodes a protein kinase required for checkpoint-mediated cell cycle arrest in response to DNA damage. Mutants of U. maydis deleted of Chk1 are severely incapacitated in RUS.

This work builds upon our previous “repopulation upon shattering” (RUS) studies in the yeast-like microbe Ustilago maydis, focusing mainly on a deeper understanding of the suicidal type of death caused by self-generated hypoxia (SGH). The key findings are: (1) the massive loss of viability induced by SGH occurs via programmed cell death (PCD), (2) the PCD-released materials are more beneficial for the surviving cells than the nutrients liberated from cells that die through necrotic processes, (3) products of PCD can stimulate growth even in the presence of growth-suppressive necromass, (4) the beneficial effects of substances released through PCD extend to two other species within the family Ustilaginaceae, and (5) U. maydis exhibited a remarkable ability to withstand the negative effects of non-PCD necromass. The third and fifth points are of special note. The third indicates that PCD-derived materials are essential for critical initial regrowth in post-stress environments where there is a high presence of non-PCD necromass. As the revitalized population strengthens, it would correspondingly enhance the communal ability to exploit more challenging nutrients. The robust resilience of U. maydis survivors against non-PCD necromass could represent an important fitness determinant, mediating competitive success in mixed microbial communities where non-PCD necromass imposes selective pressure. Thus, while providing valuable insights, the study also underscores the need for further research, especially in understanding the molecular underpinnings of the RUS phenomenon.

This work builds upon our previous “repopulation upon shattering” (RUS) studies in the yeast-like microbe Ustilago maydis, focusing mainly on a deeper understanding of the suicidal type of death caused by self-generated hypoxia (SGH). The key findings are: 1) the massive loss of viability induced by SGH occurs via programmed cell death (PCD), 2) the PCD-released materials are more beneficial for the surviving cells than the nutrients liberated from cells that die through necrotic processes, 3) products of PCD can stimulate growth even in the presence of growth-suppressive necromass, and 4) the beneficial effects of substances released through PCD extend to two other species within the family Ustilaginaceae. Additionally, U. maydis exhibited a remarkable ability to withstand the negative effects of non-PCD necromass. These results suggest PCD-released materials are essential for critical initial regrowth in post-stress environments where there is a high presence of non-PCD necromass. As the revitalized population strengthens, it would correspondingly enhance the communal ability to exploit more challenging nutrients. Alongside with the robust resilience of U. maydis survivors against non-PCD necromass, the PCD mode of dying may improve the fitness of this microorganism in harsh and fluctuating environments, warranting further investigation.