Dataset Information

The piRNA pathway responds to environmental signals to establish intergenerational adaptation to stress.

ABSTRACT:

Background

piRNAs have a constitutive role in genome defence by silencing transposable elements in the germline. In the nematode Caenorhabditis elegans, piRNAs also induce epigenetic silencing of transgenes, which can be maintained for many generations in the absence of the piRNA pathway. The role of multi-generational epigenetic inheritance in adaptation to the environment is unknown.

Results

Here, we show that piRNA biogenesis is downregulated in response to a small increase in temperature. Some effects on gene expression persist into subsequent generations and are associated with a negative fitness cost. We show that simultaneous infection with pathogenic bacteria suppresses downregulation of the piRNA pathway in response to increased temperature. This effect is associated with increased fitness of progeny of infected animals in subsequent generations.

Conclusions

Our results show that the piRNA pathway integrates inputs from the environment to establish intergenerational responses to environmental conditions, with important consequences for the fitness of the subsequent generation.

SUBMITTER: Belicard T

PROVIDER: S-EPMC6145337 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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Publications

The piRNA pathway responds to environmental signals to establish intergenerational adaptation to stress.

Belicard Tony T Jareosettasin Pree P Sarkies Peter P

BMC biology 20180918 1

<h4>Background</h4>piRNAs have a constitutive role in genome defence by silencing transposable elements in the germline. In the nematode Caenorhabditis elegans, piRNAs also induce epigenetic silencing of transgenes, which can be maintained for many generations in the absence of the piRNA pathway. The role of multi-generational epigenetic inheritance in adaptation to the environment is unknown.<h4>Results</h4>Here, we show that piRNA biogenesis is downregulated in response to a small increase in ...[more]

PMID: 30227863

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Project description:Enteropathogenic bacteria express two-component systems (TCSs) to sense and respond to host environments, developing resistance to host innate immune systems like cationic antimicrobial peptides (CAMPs). Although an opportunistic human pathogen Vibrio vulnificus shows intrinsic resistance to the CAMP-like polymyxin B (PMB), its TCSs responsible for resistance have barely been investigated. Here, a mutant exhibiting a reduced growth rate in the presence of PMB was screened from a random transposon mutant library of V. vulnificus, and response regulator CarR of the CarRS TCS was identified as essential for its PMB resistance. Transcriptome analysis revealed that CarR strongly activates the expression of the eptA, tolCV2, and carRS operons. In particular, the eptA operon plays a major role in developing the CarR-mediated PMB resistance. Phosphorylation of CarR by the sensor kinase CarS is required for the regulation of its downstream genes, leading to the PMB resistance. Nevertheless, CarR directly binds to specific sequences in the upstream regions of the eptA and carRS operons, regardless of its phosphorylation. Notably, the CarRS TCS alters its own activation state by responding to several environmental stresses, including PMB, divalent cations, bile salts, and pH change. Furthermore, CarR modulates the resistance of V. vulnificus to bile salts and acidic pH among the stresses, as well as PMB. Altogether, this study suggests that the CarRS TCS, in responding to multiple host environmental signals, could provide V. vulnificus with the benefit of surviving within the host by enhancing its optimal fitness during infection. IMPORTANCE Enteropathogenic bacteria have evolved multiple TCSs to recognize and appropriately respond to host environments. CAMP is one of the inherent host barriers that the pathogens encounter during the course of infection. In this study, the CarRS TCS of V. vulnificus was found to develop resistance to PMB, a CAMP-like antimicrobial peptide, by directly activating the expression of the eptA operon. Although CarR binds to the upstream regions of the eptA and carRS operons regardless of phosphorylation, phosphorylation of CarR is required for the regulation of the operons, resulting in the PMB resistance. Furthermore, the CarRS TCS determines the resistance of V. vulnificus to bile salts and acidic pH by differentially regulating its own activation state in response to these environmental stresses. Altogether, the CarRS TCS responds to multiple host-related signals, and thus could enhance the survival of V. vulnificus within the host, leading to successful infection.

Dataset Information

The piRNA pathway responds to environmental signals to establish intergenerational adaptation to stress.

Background

Results

Conclusions

Publications

The piRNA pathway responds to environmental signals to establish intergenerational adaptation to stress.

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