The Phenotypic Analysis of Lactobacillus plantarum shsp Mutants Reveals a Potential Role for hsp1 in Cryotolerance
Small heat shock proteins (sHSPs) are ubiquitous, low molecular weight (MW) proteins that share a conserved alpha-crystallin domain. sHSPs oligomers exhibit chaperon-like activities by interacting with unfolded substrates, thereby preventing their aggregation and precipitation. Unlike most lactobaci...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-04-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.00838/full |
| _version_ | 1828529916470099968 |
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| author | Mattia Pia Arena Vittorio Capozzi Angela Longo Pasquale Russo Stephanie Weidmann Aurélie Rieu Jean Guzzo Giuseppe Spano Daniela Fiocco |
| author_facet | Mattia Pia Arena Vittorio Capozzi Angela Longo Pasquale Russo Stephanie Weidmann Aurélie Rieu Jean Guzzo Giuseppe Spano Daniela Fiocco |
| author_sort | Mattia Pia Arena |
| collection | DOAJ |
| description | Small heat shock proteins (sHSPs) are ubiquitous, low molecular weight (MW) proteins that share a conserved alpha-crystallin domain. sHSPs oligomers exhibit chaperon-like activities by interacting with unfolded substrates, thereby preventing their aggregation and precipitation. Unlike most lactobacilli, which have single shsp genes, three different sHSP-encoding genes, i.e., hsp1, hsp2, and hsp3, were previously identified in the probiotic Lactobacillus plantarum WCFS1. Early studies, including the characterization of the knock out (KO) mutant for hsp2, indicated a different organization and transcriptional regulation of these genes and suggested that the three L. plantarum sHSPs might accomplish different tasks in stress response. To unravel the role of sHSPs, KO mutants of hsp1 and hsp3 were generated using a Cre-lox based system. Mutation of either genes resulted in impaired growth capacity under normal conditions, heat-stress and stresses typically found during host interactions and food technological process. However, survival to heat shock and the level of thermal stabilization of cytoplasmic proteins were similar between mutants and parental strain. Transcriptional analysis revealed that in the mutant genetic backgrounds there is an upregulated basal expression of the un-mutated mate hsps and other stress-related genes, which may compensate for the loss of HSP function, hence possibly accounting for the lack of a remarkable susceptibility to heat challenge. HSP3 seemed relevant for the induction of thermotolerance, while HSP1 was required for improved cryotolerance. Cell surface properties and plasma membrane fluidity were investigated to ascertain the possible membrane association of sHSP. Intriguingly, the loss of hsp1 was associated to a lower level of maximal membrane fluidity upon heat stress. A role for HSP1 in controlling and improving membrane fluidity is suggested which may pertains its cryoprotective function. |
| first_indexed | 2024-12-11T22:15:36Z |
| format | Article |
| id | doaj.art-adc1a94b60034803ad5f3367856348e2 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-11T22:15:36Z |
| publishDate | 2019-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-adc1a94b60034803ad5f3367856348e22022-12-22T00:48:37ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-04-011010.3389/fmicb.2019.00838448495The Phenotypic Analysis of Lactobacillus plantarum shsp Mutants Reveals a Potential Role for hsp1 in CryotoleranceMattia Pia Arena0Vittorio Capozzi1Angela Longo2Pasquale Russo3Stephanie Weidmann4Aurélie Rieu5Jean Guzzo6Giuseppe Spano7Daniela Fiocco8Department of Agriculture, Food and Environment Sciences, University of Foggia, Foggia, ItalyDepartment of Agriculture, Food and Environment Sciences, University of Foggia, Foggia, ItalyDepartment of Agriculture, Food and Environment Sciences, University of Foggia, Foggia, ItalyDepartment of Agriculture, Food and Environment Sciences, University of Foggia, Foggia, ItalyUniv. Bourgogne Franche-comté, AgroSup Dijon, PAM UMR A 02.102, Dijon, FranceUniv. Bourgogne Franche-comté, AgroSup Dijon, PAM UMR A 02.102, Dijon, FranceUniv. Bourgogne Franche-comté, AgroSup Dijon, PAM UMR A 02.102, Dijon, FranceDepartment of Agriculture, Food and Environment Sciences, University of Foggia, Foggia, ItalyDepartment of Clinical and Experimental Medicine, University of Foggia, Foggia, ItalySmall heat shock proteins (sHSPs) are ubiquitous, low molecular weight (MW) proteins that share a conserved alpha-crystallin domain. sHSPs oligomers exhibit chaperon-like activities by interacting with unfolded substrates, thereby preventing their aggregation and precipitation. Unlike most lactobacilli, which have single shsp genes, three different sHSP-encoding genes, i.e., hsp1, hsp2, and hsp3, were previously identified in the probiotic Lactobacillus plantarum WCFS1. Early studies, including the characterization of the knock out (KO) mutant for hsp2, indicated a different organization and transcriptional regulation of these genes and suggested that the three L. plantarum sHSPs might accomplish different tasks in stress response. To unravel the role of sHSPs, KO mutants of hsp1 and hsp3 were generated using a Cre-lox based system. Mutation of either genes resulted in impaired growth capacity under normal conditions, heat-stress and stresses typically found during host interactions and food technological process. However, survival to heat shock and the level of thermal stabilization of cytoplasmic proteins were similar between mutants and parental strain. Transcriptional analysis revealed that in the mutant genetic backgrounds there is an upregulated basal expression of the un-mutated mate hsps and other stress-related genes, which may compensate for the loss of HSP function, hence possibly accounting for the lack of a remarkable susceptibility to heat challenge. HSP3 seemed relevant for the induction of thermotolerance, while HSP1 was required for improved cryotolerance. Cell surface properties and plasma membrane fluidity were investigated to ascertain the possible membrane association of sHSP. Intriguingly, the loss of hsp1 was associated to a lower level of maximal membrane fluidity upon heat stress. A role for HSP1 in controlling and improving membrane fluidity is suggested which may pertains its cryoprotective function.https://www.frontiersin.org/article/10.3389/fmicb.2019.00838/fullsmall heat shock proteins (sHSP)chaperoneLactobacillus plantarumprobioticstressmembrane fluidity |
| spellingShingle | Mattia Pia Arena Vittorio Capozzi Angela Longo Pasquale Russo Stephanie Weidmann Aurélie Rieu Jean Guzzo Giuseppe Spano Daniela Fiocco The Phenotypic Analysis of Lactobacillus plantarum shsp Mutants Reveals a Potential Role for hsp1 in Cryotolerance Frontiers in Microbiology small heat shock proteins (sHSP) chaperone Lactobacillus plantarum probiotic stress membrane fluidity |
| title | The Phenotypic Analysis of Lactobacillus plantarum shsp Mutants Reveals a Potential Role for hsp1 in Cryotolerance |
| title_full | The Phenotypic Analysis of Lactobacillus plantarum shsp Mutants Reveals a Potential Role for hsp1 in Cryotolerance |
| title_fullStr | The Phenotypic Analysis of Lactobacillus plantarum shsp Mutants Reveals a Potential Role for hsp1 in Cryotolerance |
| title_full_unstemmed | The Phenotypic Analysis of Lactobacillus plantarum shsp Mutants Reveals a Potential Role for hsp1 in Cryotolerance |
| title_short | The Phenotypic Analysis of Lactobacillus plantarum shsp Mutants Reveals a Potential Role for hsp1 in Cryotolerance |
| title_sort | phenotypic analysis of lactobacillus plantarum shsp mutants reveals a potential role for hsp1 in cryotolerance |
| topic | small heat shock proteins (sHSP) chaperone Lactobacillus plantarum probiotic stress membrane fluidity |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.00838/full |
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