Generation of Distinct Differentially Culturable Forms of Burkholderia following Starvation at Low Temperature

ABSTRACT Bacteria have developed unique mechanisms to adapt to environmental stresses and challenges of the immune system. Here, we report that Burkholderia pseudomallei, the causative agent of melioidosis, and its laboratory surrogate, Burkholderia thailandensis, utilize distinct mechanisms for surviving starvation at different incubation temperatures. At 21°C, Burkholderia are present as short rods which can rapidly reactivate and form colonies on solid media. At 4°C, Burkholderia convert into coccoid forms that cannot be cultured on solid agar but can be resuscitated in liquid media supplemented with supernatant obtained from logarithmic phase cultures of B. thailandensis, or catalase and Tween 80, thus displaying characteristics of differentially culturable bacteria (DCB). These DCB have low intensity fluorescence when stained with SYTO 9, have an intact cell membrane (propidium iodide negative), and contain 16S rRNA at levels comparable with growing cells. We also present evidence that lytic transglycosylases, a family of peptidoglycan-remodeling enzymes, are involved in the generation of coccoid forms and their resuscitation to actively growing cells. A B. pseudomallei ΔltgGCFD mutant with four ltg genes deleted did not produce coccoid forms at 4°C and could not be resuscitated in the liquid media evaluated. Our findings provide insights into the adaptation of Burkholderia to nutrient limitation and the generation of differentially culturable bacteria. IMPORTANCE Bacterial pathogens exhibit physiologically distinct forms that enable their survival in an infected host, the environment and following exposure to antimicrobial agents. B. pseudomallei causes the disease melioidosis, which has a high mortality rate and is difficult to treat with antibiotics. The bacterium is endemic to several countries and detected in high abundance in the environment. Here, we report that during starvation at low temperature, B. pseudomallei produces coccoid forms that cannot grow in standard media and which, therefore, can be challenging to detect using common tools. We provide evidence that the formation of these cocci is mediated by cell wall-specialized enzymes and lytic transglycosylases, and that resuscitation of these forms occurs following the addition of catalase and Tween 80. Our findings have important implications for the disease control and detection of B. pseudomallei, an agent of both public health and defense interest. Ausführliche Beschreibung

Gespeichert in:

Autor*in:	Joss M. Auty [verfasserIn] Christopher H. Jenkins [verfasserIn] Jennifer Hincks [verfasserIn] Anna A. Straatman-Iwanowska [verfasserIn] Natalie Allcock [verfasserIn] Obolbek Turapov [verfasserIn] Edouard E. Galyov [verfasserIn] Sarah V. Harding [verfasserIn] Galina V. Mukamolova [verfasserIn]

Format:	E-Artikel
Sprache:	Englisch

Erschienen:	2022

Schlagwörter:	Burkholderia pseudomallei Burkholderia thailandensis differentially culturable cells lytic transglycosylase coccoid cells resuscitation

Übergeordnetes Werk:	In: Microbiology Spectrum - American Society for Microbiology, 2022, 10(2022), 1
Übergeordnetes Werk:	volume:10 ; year:2022 ; number:1

Links:	Link aufrufen Link aufrufen Link aufrufen Journal toc

DOI / URN:	10.1128/spectrum.02110-21

Katalog-ID:	DOAJ016988787

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allfields	10.1128/spectrum.02110-21 doi (DE-627)DOAJ016988787 (DE-599)DOAJfbc42d0f12be494abe7d5a68c8bacc75 DE-627 ger DE-627 rakwb eng QR1-502 Joss M. Auty verfasserin aut Generation of Distinct Differentially Culturable Forms of Burkholderia following Starvation at Low Temperature 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Bacteria have developed unique mechanisms to adapt to environmental stresses and challenges of the immune system. Here, we report that Burkholderia pseudomallei, the causative agent of melioidosis, and its laboratory surrogate, Burkholderia thailandensis, utilize distinct mechanisms for surviving starvation at different incubation temperatures. At 21°C, Burkholderia are present as short rods which can rapidly reactivate and form colonies on solid media. At 4°C, Burkholderia convert into coccoid forms that cannot be cultured on solid agar but can be resuscitated in liquid media supplemented with supernatant obtained from logarithmic phase cultures of B. thailandensis, or catalase and Tween 80, thus displaying characteristics of differentially culturable bacteria (DCB). These DCB have low intensity fluorescence when stained with SYTO 9, have an intact cell membrane (propidium iodide negative), and contain 16S rRNA at levels comparable with growing cells. We also present evidence that lytic transglycosylases, a family of peptidoglycan-remodeling enzymes, are involved in the generation of coccoid forms and their resuscitation to actively growing cells. A B. pseudomallei ΔltgGCFD mutant with four ltg genes deleted did not produce coccoid forms at 4°C and could not be resuscitated in the liquid media evaluated. Our findings provide insights into the adaptation of Burkholderia to nutrient limitation and the generation of differentially culturable bacteria. IMPORTANCE Bacterial pathogens exhibit physiologically distinct forms that enable their survival in an infected host, the environment and following exposure to antimicrobial agents. B. pseudomallei causes the disease melioidosis, which has a high mortality rate and is difficult to treat with antibiotics. The bacterium is endemic to several countries and detected in high abundance in the environment. Here, we report that during starvation at low temperature, B. pseudomallei produces coccoid forms that cannot grow in standard media and which, therefore, can be challenging to detect using common tools. We provide evidence that the formation of these cocci is mediated by cell wall-specialized enzymes and lytic transglycosylases, and that resuscitation of these forms occurs following the addition of catalase and Tween 80. Our findings have important implications for the disease control and detection of B. pseudomallei, an agent of both public health and defense interest. Burkholderia pseudomallei Burkholderia thailandensis differentially culturable cells lytic transglycosylase coccoid cells resuscitation Microbiology Christopher H. Jenkins verfasserin aut Jennifer Hincks verfasserin aut Anna A. Straatman-Iwanowska verfasserin aut Natalie Allcock verfasserin aut Obolbek Turapov verfasserin aut Edouard E. Galyov verfasserin aut Sarah V. Harding verfasserin aut Galina V. Mukamolova verfasserin aut In Microbiology Spectrum American Society for Microbiology, 2022 10(2022), 1 (DE-627)816693293 (DE-600)2807133-5 21650497 nnns volume:10 year:2022 number:1 https://doi.org/10.1128/spectrum.02110-21 kostenfrei https://doaj.org/article/fbc42d0f12be494abe7d5a68c8bacc75 kostenfrei https://journals.asm.org/doi/10.1128/spectrum.02110-21 kostenfrei https://doaj.org/toc/2165-0497 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ SSG-OLC-PHA GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_120 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_252 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 10 2022 1
spelling	10.1128/spectrum.02110-21 doi (DE-627)DOAJ016988787 (DE-599)DOAJfbc42d0f12be494abe7d5a68c8bacc75 DE-627 ger DE-627 rakwb eng QR1-502 Joss M. Auty verfasserin aut Generation of Distinct Differentially Culturable Forms of Burkholderia following Starvation at Low Temperature 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Bacteria have developed unique mechanisms to adapt to environmental stresses and challenges of the immune system. Here, we report that Burkholderia pseudomallei, the causative agent of melioidosis, and its laboratory surrogate, Burkholderia thailandensis, utilize distinct mechanisms for surviving starvation at different incubation temperatures. At 21°C, Burkholderia are present as short rods which can rapidly reactivate and form colonies on solid media. At 4°C, Burkholderia convert into coccoid forms that cannot be cultured on solid agar but can be resuscitated in liquid media supplemented with supernatant obtained from logarithmic phase cultures of B. thailandensis, or catalase and Tween 80, thus displaying characteristics of differentially culturable bacteria (DCB). These DCB have low intensity fluorescence when stained with SYTO 9, have an intact cell membrane (propidium iodide negative), and contain 16S rRNA at levels comparable with growing cells. We also present evidence that lytic transglycosylases, a family of peptidoglycan-remodeling enzymes, are involved in the generation of coccoid forms and their resuscitation to actively growing cells. A B. pseudomallei ΔltgGCFD mutant with four ltg genes deleted did not produce coccoid forms at 4°C and could not be resuscitated in the liquid media evaluated. Our findings provide insights into the adaptation of Burkholderia to nutrient limitation and the generation of differentially culturable bacteria. IMPORTANCE Bacterial pathogens exhibit physiologically distinct forms that enable their survival in an infected host, the environment and following exposure to antimicrobial agents. B. pseudomallei causes the disease melioidosis, which has a high mortality rate and is difficult to treat with antibiotics. The bacterium is endemic to several countries and detected in high abundance in the environment. Here, we report that during starvation at low temperature, B. pseudomallei produces coccoid forms that cannot grow in standard media and which, therefore, can be challenging to detect using common tools. We provide evidence that the formation of these cocci is mediated by cell wall-specialized enzymes and lytic transglycosylases, and that resuscitation of these forms occurs following the addition of catalase and Tween 80. Our findings have important implications for the disease control and detection of B. pseudomallei, an agent of both public health and defense interest. Burkholderia pseudomallei Burkholderia thailandensis differentially culturable cells lytic transglycosylase coccoid cells resuscitation Microbiology Christopher H. Jenkins verfasserin aut Jennifer Hincks verfasserin aut Anna A. Straatman-Iwanowska verfasserin aut Natalie Allcock verfasserin aut Obolbek Turapov verfasserin aut Edouard E. Galyov verfasserin aut Sarah V. Harding verfasserin aut Galina V. Mukamolova verfasserin aut In Microbiology Spectrum American Society for Microbiology, 2022 10(2022), 1 (DE-627)816693293 (DE-600)2807133-5 21650497 nnns volume:10 year:2022 number:1 https://doi.org/10.1128/spectrum.02110-21 kostenfrei https://doaj.org/article/fbc42d0f12be494abe7d5a68c8bacc75 kostenfrei https://journals.asm.org/doi/10.1128/spectrum.02110-21 kostenfrei https://doaj.org/toc/2165-0497 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ SSG-OLC-PHA GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_120 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_252 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 10 2022 1
allfields_unstemmed	10.1128/spectrum.02110-21 doi (DE-627)DOAJ016988787 (DE-599)DOAJfbc42d0f12be494abe7d5a68c8bacc75 DE-627 ger DE-627 rakwb eng QR1-502 Joss M. Auty verfasserin aut Generation of Distinct Differentially Culturable Forms of Burkholderia following Starvation at Low Temperature 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Bacteria have developed unique mechanisms to adapt to environmental stresses and challenges of the immune system. Here, we report that Burkholderia pseudomallei, the causative agent of melioidosis, and its laboratory surrogate, Burkholderia thailandensis, utilize distinct mechanisms for surviving starvation at different incubation temperatures. At 21°C, Burkholderia are present as short rods which can rapidly reactivate and form colonies on solid media. At 4°C, Burkholderia convert into coccoid forms that cannot be cultured on solid agar but can be resuscitated in liquid media supplemented with supernatant obtained from logarithmic phase cultures of B. thailandensis, or catalase and Tween 80, thus displaying characteristics of differentially culturable bacteria (DCB). These DCB have low intensity fluorescence when stained with SYTO 9, have an intact cell membrane (propidium iodide negative), and contain 16S rRNA at levels comparable with growing cells. We also present evidence that lytic transglycosylases, a family of peptidoglycan-remodeling enzymes, are involved in the generation of coccoid forms and their resuscitation to actively growing cells. A B. pseudomallei ΔltgGCFD mutant with four ltg genes deleted did not produce coccoid forms at 4°C and could not be resuscitated in the liquid media evaluated. Our findings provide insights into the adaptation of Burkholderia to nutrient limitation and the generation of differentially culturable bacteria. IMPORTANCE Bacterial pathogens exhibit physiologically distinct forms that enable their survival in an infected host, the environment and following exposure to antimicrobial agents. B. pseudomallei causes the disease melioidosis, which has a high mortality rate and is difficult to treat with antibiotics. The bacterium is endemic to several countries and detected in high abundance in the environment. Here, we report that during starvation at low temperature, B. pseudomallei produces coccoid forms that cannot grow in standard media and which, therefore, can be challenging to detect using common tools. We provide evidence that the formation of these cocci is mediated by cell wall-specialized enzymes and lytic transglycosylases, and that resuscitation of these forms occurs following the addition of catalase and Tween 80. Our findings have important implications for the disease control and detection of B. pseudomallei, an agent of both public health and defense interest. Burkholderia pseudomallei Burkholderia thailandensis differentially culturable cells lytic transglycosylase coccoid cells resuscitation Microbiology Christopher H. Jenkins verfasserin aut Jennifer Hincks verfasserin aut Anna A. Straatman-Iwanowska verfasserin aut Natalie Allcock verfasserin aut Obolbek Turapov verfasserin aut Edouard E. Galyov verfasserin aut Sarah V. Harding verfasserin aut Galina V. Mukamolova verfasserin aut In Microbiology Spectrum American Society for Microbiology, 2022 10(2022), 1 (DE-627)816693293 (DE-600)2807133-5 21650497 nnns volume:10 year:2022 number:1 https://doi.org/10.1128/spectrum.02110-21 kostenfrei https://doaj.org/article/fbc42d0f12be494abe7d5a68c8bacc75 kostenfrei https://journals.asm.org/doi/10.1128/spectrum.02110-21 kostenfrei https://doaj.org/toc/2165-0497 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ SSG-OLC-PHA GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_120 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_252 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 10 2022 1
allfieldsGer	10.1128/spectrum.02110-21 doi (DE-627)DOAJ016988787 (DE-599)DOAJfbc42d0f12be494abe7d5a68c8bacc75 DE-627 ger DE-627 rakwb eng QR1-502 Joss M. Auty verfasserin aut Generation of Distinct Differentially Culturable Forms of Burkholderia following Starvation at Low Temperature 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Bacteria have developed unique mechanisms to adapt to environmental stresses and challenges of the immune system. Here, we report that Burkholderia pseudomallei, the causative agent of melioidosis, and its laboratory surrogate, Burkholderia thailandensis, utilize distinct mechanisms for surviving starvation at different incubation temperatures. At 21°C, Burkholderia are present as short rods which can rapidly reactivate and form colonies on solid media. At 4°C, Burkholderia convert into coccoid forms that cannot be cultured on solid agar but can be resuscitated in liquid media supplemented with supernatant obtained from logarithmic phase cultures of B. thailandensis, or catalase and Tween 80, thus displaying characteristics of differentially culturable bacteria (DCB). These DCB have low intensity fluorescence when stained with SYTO 9, have an intact cell membrane (propidium iodide negative), and contain 16S rRNA at levels comparable with growing cells. We also present evidence that lytic transglycosylases, a family of peptidoglycan-remodeling enzymes, are involved in the generation of coccoid forms and their resuscitation to actively growing cells. A B. pseudomallei ΔltgGCFD mutant with four ltg genes deleted did not produce coccoid forms at 4°C and could not be resuscitated in the liquid media evaluated. Our findings provide insights into the adaptation of Burkholderia to nutrient limitation and the generation of differentially culturable bacteria. IMPORTANCE Bacterial pathogens exhibit physiologically distinct forms that enable their survival in an infected host, the environment and following exposure to antimicrobial agents. B. pseudomallei causes the disease melioidosis, which has a high mortality rate and is difficult to treat with antibiotics. The bacterium is endemic to several countries and detected in high abundance in the environment. Here, we report that during starvation at low temperature, B. pseudomallei produces coccoid forms that cannot grow in standard media and which, therefore, can be challenging to detect using common tools. We provide evidence that the formation of these cocci is mediated by cell wall-specialized enzymes and lytic transglycosylases, and that resuscitation of these forms occurs following the addition of catalase and Tween 80. Our findings have important implications for the disease control and detection of B. pseudomallei, an agent of both public health and defense interest. Burkholderia pseudomallei Burkholderia thailandensis differentially culturable cells lytic transglycosylase coccoid cells resuscitation Microbiology Christopher H. Jenkins verfasserin aut Jennifer Hincks verfasserin aut Anna A. Straatman-Iwanowska verfasserin aut Natalie Allcock verfasserin aut Obolbek Turapov verfasserin aut Edouard E. Galyov verfasserin aut Sarah V. Harding verfasserin aut Galina V. Mukamolova verfasserin aut In Microbiology Spectrum American Society for Microbiology, 2022 10(2022), 1 (DE-627)816693293 (DE-600)2807133-5 21650497 nnns volume:10 year:2022 number:1 https://doi.org/10.1128/spectrum.02110-21 kostenfrei https://doaj.org/article/fbc42d0f12be494abe7d5a68c8bacc75 kostenfrei https://journals.asm.org/doi/10.1128/spectrum.02110-21 kostenfrei https://doaj.org/toc/2165-0497 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ SSG-OLC-PHA GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_120 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_252 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 10 2022 1
allfieldsSound	10.1128/spectrum.02110-21 doi (DE-627)DOAJ016988787 (DE-599)DOAJfbc42d0f12be494abe7d5a68c8bacc75 DE-627 ger DE-627 rakwb eng QR1-502 Joss M. Auty verfasserin aut Generation of Distinct Differentially Culturable Forms of Burkholderia following Starvation at Low Temperature 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Bacteria have developed unique mechanisms to adapt to environmental stresses and challenges of the immune system. Here, we report that Burkholderia pseudomallei, the causative agent of melioidosis, and its laboratory surrogate, Burkholderia thailandensis, utilize distinct mechanisms for surviving starvation at different incubation temperatures. At 21°C, Burkholderia are present as short rods which can rapidly reactivate and form colonies on solid media. At 4°C, Burkholderia convert into coccoid forms that cannot be cultured on solid agar but can be resuscitated in liquid media supplemented with supernatant obtained from logarithmic phase cultures of B. thailandensis, or catalase and Tween 80, thus displaying characteristics of differentially culturable bacteria (DCB). These DCB have low intensity fluorescence when stained with SYTO 9, have an intact cell membrane (propidium iodide negative), and contain 16S rRNA at levels comparable with growing cells. We also present evidence that lytic transglycosylases, a family of peptidoglycan-remodeling enzymes, are involved in the generation of coccoid forms and their resuscitation to actively growing cells. A B. pseudomallei ΔltgGCFD mutant with four ltg genes deleted did not produce coccoid forms at 4°C and could not be resuscitated in the liquid media evaluated. Our findings provide insights into the adaptation of Burkholderia to nutrient limitation and the generation of differentially culturable bacteria. IMPORTANCE Bacterial pathogens exhibit physiologically distinct forms that enable their survival in an infected host, the environment and following exposure to antimicrobial agents. B. pseudomallei causes the disease melioidosis, which has a high mortality rate and is difficult to treat with antibiotics. The bacterium is endemic to several countries and detected in high abundance in the environment. Here, we report that during starvation at low temperature, B. pseudomallei produces coccoid forms that cannot grow in standard media and which, therefore, can be challenging to detect using common tools. We provide evidence that the formation of these cocci is mediated by cell wall-specialized enzymes and lytic transglycosylases, and that resuscitation of these forms occurs following the addition of catalase and Tween 80. Our findings have important implications for the disease control and detection of B. pseudomallei, an agent of both public health and defense interest. Burkholderia pseudomallei Burkholderia thailandensis differentially culturable cells lytic transglycosylase coccoid cells resuscitation Microbiology Christopher H. Jenkins verfasserin aut Jennifer Hincks verfasserin aut Anna A. Straatman-Iwanowska verfasserin aut Natalie Allcock verfasserin aut Obolbek Turapov verfasserin aut Edouard E. Galyov verfasserin aut Sarah V. Harding verfasserin aut Galina V. Mukamolova verfasserin aut In Microbiology Spectrum American Society for Microbiology, 2022 10(2022), 1 (DE-627)816693293 (DE-600)2807133-5 21650497 nnns volume:10 year:2022 number:1 https://doi.org/10.1128/spectrum.02110-21 kostenfrei https://doaj.org/article/fbc42d0f12be494abe7d5a68c8bacc75 kostenfrei https://journals.asm.org/doi/10.1128/spectrum.02110-21 kostenfrei https://doaj.org/toc/2165-0497 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ SSG-OLC-PHA GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_120 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_252 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 10 2022 1
language	English
source	In Microbiology Spectrum 10(2022), 1 volume:10 year:2022 number:1
sourceStr	In Microbiology Spectrum 10(2022), 1 volume:10 year:2022 number:1
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institution	findex.gbv.de
topic_facet	Burkholderia pseudomallei Burkholderia thailandensis differentially culturable cells lytic transglycosylase coccoid cells resuscitation Microbiology
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container_title	Microbiology Spectrum
authorswithroles_txt_mv	Joss M. Auty @@aut@@ Christopher H. Jenkins @@aut@@ Jennifer Hincks @@aut@@ Anna A. Straatman-Iwanowska @@aut@@ Natalie Allcock @@aut@@ Obolbek Turapov @@aut@@ Edouard E. Galyov @@aut@@ Sarah V. Harding @@aut@@ Galina V. Mukamolova @@aut@@
publishDateDaySort_date	2022-01-01T00:00:00Z
hierarchy_top_id	816693293
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callnumber-first	Q - Science
author	Joss M. Auty
spellingShingle	Joss M. Auty misc QR1-502 misc Burkholderia pseudomallei misc Burkholderia thailandensis misc differentially culturable cells misc lytic transglycosylase misc coccoid cells misc resuscitation misc Microbiology Generation of Distinct Differentially Culturable Forms of Burkholderia following Starvation at Low Temperature
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topic_title	QR1-502 Generation of Distinct Differentially Culturable Forms of Burkholderia following Starvation at Low Temperature Burkholderia pseudomallei Burkholderia thailandensis differentially culturable cells lytic transglycosylase coccoid cells resuscitation
topic	misc QR1-502 misc Burkholderia pseudomallei misc Burkholderia thailandensis misc differentially culturable cells misc lytic transglycosylase misc coccoid cells misc resuscitation misc Microbiology
topic_unstemmed	misc QR1-502 misc Burkholderia pseudomallei misc Burkholderia thailandensis misc differentially culturable cells misc lytic transglycosylase misc coccoid cells misc resuscitation misc Microbiology
topic_browse	misc QR1-502 misc Burkholderia pseudomallei misc Burkholderia thailandensis misc differentially culturable cells misc lytic transglycosylase misc coccoid cells misc resuscitation misc Microbiology
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title	Generation of Distinct Differentially Culturable Forms of Burkholderia following Starvation at Low Temperature
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title_full	Generation of Distinct Differentially Culturable Forms of Burkholderia following Starvation at Low Temperature
author_sort	Joss M. Auty
journal	Microbiology Spectrum
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author_browse	Joss M. Auty Christopher H. Jenkins Jennifer Hincks Anna A. Straatman-Iwanowska Natalie Allcock Obolbek Turapov Edouard E. Galyov Sarah V. Harding Galina V. Mukamolova
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doi_str_mv	10.1128/spectrum.02110-21
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title_sort	generation of distinct differentially culturable forms of burkholderia following starvation at low temperature
callnumber	QR1-502
title_auth	Generation of Distinct Differentially Culturable Forms of Burkholderia following Starvation at Low Temperature
abstract	ABSTRACT Bacteria have developed unique mechanisms to adapt to environmental stresses and challenges of the immune system. Here, we report that Burkholderia pseudomallei, the causative agent of melioidosis, and its laboratory surrogate, Burkholderia thailandensis, utilize distinct mechanisms for surviving starvation at different incubation temperatures. At 21°C, Burkholderia are present as short rods which can rapidly reactivate and form colonies on solid media. At 4°C, Burkholderia convert into coccoid forms that cannot be cultured on solid agar but can be resuscitated in liquid media supplemented with supernatant obtained from logarithmic phase cultures of B. thailandensis, or catalase and Tween 80, thus displaying characteristics of differentially culturable bacteria (DCB). These DCB have low intensity fluorescence when stained with SYTO 9, have an intact cell membrane (propidium iodide negative), and contain 16S rRNA at levels comparable with growing cells. We also present evidence that lytic transglycosylases, a family of peptidoglycan-remodeling enzymes, are involved in the generation of coccoid forms and their resuscitation to actively growing cells. A B. pseudomallei ΔltgGCFD mutant with four ltg genes deleted did not produce coccoid forms at 4°C and could not be resuscitated in the liquid media evaluated. Our findings provide insights into the adaptation of Burkholderia to nutrient limitation and the generation of differentially culturable bacteria. IMPORTANCE Bacterial pathogens exhibit physiologically distinct forms that enable their survival in an infected host, the environment and following exposure to antimicrobial agents. B. pseudomallei causes the disease melioidosis, which has a high mortality rate and is difficult to treat with antibiotics. The bacterium is endemic to several countries and detected in high abundance in the environment. Here, we report that during starvation at low temperature, B. pseudomallei produces coccoid forms that cannot grow in standard media and which, therefore, can be challenging to detect using common tools. We provide evidence that the formation of these cocci is mediated by cell wall-specialized enzymes and lytic transglycosylases, and that resuscitation of these forms occurs following the addition of catalase and Tween 80. Our findings have important implications for the disease control and detection of B. pseudomallei, an agent of both public health and defense interest.
abstractGer	ABSTRACT Bacteria have developed unique mechanisms to adapt to environmental stresses and challenges of the immune system. Here, we report that Burkholderia pseudomallei, the causative agent of melioidosis, and its laboratory surrogate, Burkholderia thailandensis, utilize distinct mechanisms for surviving starvation at different incubation temperatures. At 21°C, Burkholderia are present as short rods which can rapidly reactivate and form colonies on solid media. At 4°C, Burkholderia convert into coccoid forms that cannot be cultured on solid agar but can be resuscitated in liquid media supplemented with supernatant obtained from logarithmic phase cultures of B. thailandensis, or catalase and Tween 80, thus displaying characteristics of differentially culturable bacteria (DCB). These DCB have low intensity fluorescence when stained with SYTO 9, have an intact cell membrane (propidium iodide negative), and contain 16S rRNA at levels comparable with growing cells. We also present evidence that lytic transglycosylases, a family of peptidoglycan-remodeling enzymes, are involved in the generation of coccoid forms and their resuscitation to actively growing cells. A B. pseudomallei ΔltgGCFD mutant with four ltg genes deleted did not produce coccoid forms at 4°C and could not be resuscitated in the liquid media evaluated. Our findings provide insights into the adaptation of Burkholderia to nutrient limitation and the generation of differentially culturable bacteria. IMPORTANCE Bacterial pathogens exhibit physiologically distinct forms that enable their survival in an infected host, the environment and following exposure to antimicrobial agents. B. pseudomallei causes the disease melioidosis, which has a high mortality rate and is difficult to treat with antibiotics. The bacterium is endemic to several countries and detected in high abundance in the environment. Here, we report that during starvation at low temperature, B. pseudomallei produces coccoid forms that cannot grow in standard media and which, therefore, can be challenging to detect using common tools. We provide evidence that the formation of these cocci is mediated by cell wall-specialized enzymes and lytic transglycosylases, and that resuscitation of these forms occurs following the addition of catalase and Tween 80. Our findings have important implications for the disease control and detection of B. pseudomallei, an agent of both public health and defense interest.
abstract_unstemmed	ABSTRACT Bacteria have developed unique mechanisms to adapt to environmental stresses and challenges of the immune system. Here, we report that Burkholderia pseudomallei, the causative agent of melioidosis, and its laboratory surrogate, Burkholderia thailandensis, utilize distinct mechanisms for surviving starvation at different incubation temperatures. At 21°C, Burkholderia are present as short rods which can rapidly reactivate and form colonies on solid media. At 4°C, Burkholderia convert into coccoid forms that cannot be cultured on solid agar but can be resuscitated in liquid media supplemented with supernatant obtained from logarithmic phase cultures of B. thailandensis, or catalase and Tween 80, thus displaying characteristics of differentially culturable bacteria (DCB). These DCB have low intensity fluorescence when stained with SYTO 9, have an intact cell membrane (propidium iodide negative), and contain 16S rRNA at levels comparable with growing cells. We also present evidence that lytic transglycosylases, a family of peptidoglycan-remodeling enzymes, are involved in the generation of coccoid forms and their resuscitation to actively growing cells. A B. pseudomallei ΔltgGCFD mutant with four ltg genes deleted did not produce coccoid forms at 4°C and could not be resuscitated in the liquid media evaluated. Our findings provide insights into the adaptation of Burkholderia to nutrient limitation and the generation of differentially culturable bacteria. IMPORTANCE Bacterial pathogens exhibit physiologically distinct forms that enable their survival in an infected host, the environment and following exposure to antimicrobial agents. B. pseudomallei causes the disease melioidosis, which has a high mortality rate and is difficult to treat with antibiotics. The bacterium is endemic to several countries and detected in high abundance in the environment. Here, we report that during starvation at low temperature, B. pseudomallei produces coccoid forms that cannot grow in standard media and which, therefore, can be challenging to detect using common tools. We provide evidence that the formation of these cocci is mediated by cell wall-specialized enzymes and lytic transglycosylases, and that resuscitation of these forms occurs following the addition of catalase and Tween 80. Our findings have important implications for the disease control and detection of B. pseudomallei, an agent of both public health and defense interest.
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title_short	Generation of Distinct Differentially Culturable Forms of Burkholderia following Starvation at Low Temperature
url	https://doi.org/10.1128/spectrum.02110-21 https://doaj.org/article/fbc42d0f12be494abe7d5a68c8bacc75 https://journals.asm.org/doi/10.1128/spectrum.02110-21 https://doaj.org/toc/2165-0497
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Generation of Distinct Differentially Culturable Forms of Burkholderia following Starvation at Low Temperature

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