Memory of Germinant Stimuli in Bacterial Spores

ABSTRACT Bacterial spores, despite being metabolically dormant, possess the remarkable capacity to detect nutrients and other molecules in their environment through a biochemical sensory apparatus that can trigger spore germination, allowing the return to vegetative growth within minutes of exposure...

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Autores principales: Shiwei Wang, James R. Faeder, Peter Setlow, Yong-qing Li
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Publicado: American Society for Microbiology 2015
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Acceso en línea:https://doaj.org/article/e7663a669ade473aa7de76e086e679c6
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spelling oai:doaj.org-article:e7663a669ade473aa7de76e086e679c62021-11-15T15:41:24ZMemory of Germinant Stimuli in Bacterial Spores10.1128/mBio.01859-152150-7511https://doaj.org/article/e7663a669ade473aa7de76e086e679c62015-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01859-15https://doaj.org/toc/2150-7511ABSTRACT Bacterial spores, despite being metabolically dormant, possess the remarkable capacity to detect nutrients and other molecules in their environment through a biochemical sensory apparatus that can trigger spore germination, allowing the return to vegetative growth within minutes of exposure of germinants. We demonstrate here that bacterial spores of multiple species retain memory of transient exposures to germinant stimuli that can result in altered responses to subsequent exposure. The magnitude and decay of these memory effects depend on the pulse duration as well as on the separation time, incubation temperature, and pH values between the pulses. Spores of Bacillus species germinate in response to nutrients that interact with germinant receptors (GRs) in the spore's inner membrane, with different nutrient types acting on different receptors. In our experiments, B. subtilis spores display memory when the first and second germinant pulses target different receptors, suggesting that some components of spore memory are downstream of GRs. Furthermore, nonnutrient germinants, which do not require GRs, exhibit memory either alone or in combination with nutrient germinants, and memory of nonnutrient stimulation is found to be more persistent than that induced by GR-dependent stimuli. Spores of B. cereus and Clostridium difficile also exhibit germination memory, suggesting that memory may be a general property of bacterial spores. These observations along with experiments involving strains with mutations in various germination proteins suggest a model in which memory is stored primarily in the metastable states of SpoVA proteins, which comprise a channel for release of dipicolinic acid, a major early event in spore germination. IMPORTANCE Cellular memory is defined as a sustained response to a transient environmental stimulus, and yet its generation and storage have not been described in bacterial spores. We demonstrate here that bacterial spores of multiple species retain memory of transient exposures to germinant stimuli that can result in altered responses to subsequent exposure. Memory was induced by activation of germinant receptors (GRs) or by GR-independent germinants and was accessed by both GR-dependent and GR-independent germinants. Analysis of effects on memory of exposure to GR-dependent and GR-independent germinants as well as in spores lacking various germination proteins suggests a model in which memory is stored primarily in metastable states of SpoVA proteins which comprise a channel for release of spore dipicolinic acid. Spore memory can also significantly reduce the concentration of nutrient germinants necessary to trigger germination, and this may be used to respond to low levels of nutrient germinants.Shiwei WangJames R. FaederPeter SetlowYong-qing LiAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 6 (2015)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Shiwei Wang
James R. Faeder
Peter Setlow
Yong-qing Li
Memory of Germinant Stimuli in Bacterial Spores
description ABSTRACT Bacterial spores, despite being metabolically dormant, possess the remarkable capacity to detect nutrients and other molecules in their environment through a biochemical sensory apparatus that can trigger spore germination, allowing the return to vegetative growth within minutes of exposure of germinants. We demonstrate here that bacterial spores of multiple species retain memory of transient exposures to germinant stimuli that can result in altered responses to subsequent exposure. The magnitude and decay of these memory effects depend on the pulse duration as well as on the separation time, incubation temperature, and pH values between the pulses. Spores of Bacillus species germinate in response to nutrients that interact with germinant receptors (GRs) in the spore's inner membrane, with different nutrient types acting on different receptors. In our experiments, B. subtilis spores display memory when the first and second germinant pulses target different receptors, suggesting that some components of spore memory are downstream of GRs. Furthermore, nonnutrient germinants, which do not require GRs, exhibit memory either alone or in combination with nutrient germinants, and memory of nonnutrient stimulation is found to be more persistent than that induced by GR-dependent stimuli. Spores of B. cereus and Clostridium difficile also exhibit germination memory, suggesting that memory may be a general property of bacterial spores. These observations along with experiments involving strains with mutations in various germination proteins suggest a model in which memory is stored primarily in the metastable states of SpoVA proteins, which comprise a channel for release of dipicolinic acid, a major early event in spore germination. IMPORTANCE Cellular memory is defined as a sustained response to a transient environmental stimulus, and yet its generation and storage have not been described in bacterial spores. We demonstrate here that bacterial spores of multiple species retain memory of transient exposures to germinant stimuli that can result in altered responses to subsequent exposure. Memory was induced by activation of germinant receptors (GRs) or by GR-independent germinants and was accessed by both GR-dependent and GR-independent germinants. Analysis of effects on memory of exposure to GR-dependent and GR-independent germinants as well as in spores lacking various germination proteins suggests a model in which memory is stored primarily in metastable states of SpoVA proteins which comprise a channel for release of spore dipicolinic acid. Spore memory can also significantly reduce the concentration of nutrient germinants necessary to trigger germination, and this may be used to respond to low levels of nutrient germinants.
format article
author Shiwei Wang
James R. Faeder
Peter Setlow
Yong-qing Li
author_facet Shiwei Wang
James R. Faeder
Peter Setlow
Yong-qing Li
author_sort Shiwei Wang
title Memory of Germinant Stimuli in Bacterial Spores
title_short Memory of Germinant Stimuli in Bacterial Spores
title_full Memory of Germinant Stimuli in Bacterial Spores
title_fullStr Memory of Germinant Stimuli in Bacterial Spores
title_full_unstemmed Memory of Germinant Stimuli in Bacterial Spores
title_sort memory of germinant stimuli in bacterial spores
publisher American Society for Microbiology
publishDate 2015
url https://doaj.org/article/e7663a669ade473aa7de76e086e679c6
work_keys_str_mv AT shiweiwang memoryofgerminantstimuliinbacterialspores
AT jamesrfaeder memoryofgerminantstimuliinbacterialspores
AT petersetlow memoryofgerminantstimuliinbacterialspores
AT yongqingli memoryofgerminantstimuliinbacterialspores
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