Genome-wide survey of efflux pump-coding genes associated with Cronobacter survival, osmotic adaptation, and persistence

Flavia Negrete; Hyein Jang; Jayanthi Gangiredla; Jung Ha Woo; You Young Lee; Isha R. Patel; Hannah R. Chase; Samantha Finkelstein; Caroline Z. Wang; Shabarinath Srikumar; Scott Nguyen; Athmanya Eshwar; Roger Stephan; Angelika Lehner; Séamus Fanning; Ben D. Tall; Gopal R. Gopinath

doi:10.1016/j.cofs.2018.11.005

Genome-wide survey of efflux pump-coding genes associated with Cronobacter survival, osmotic adaptation, and persistence

Flavia Negrete, Hyein Jang, Jayanthi Gangiredla, Jung Ha Woo, You Young Lee, Isha R. Patel, Hannah R. Chase, Samantha Finkelstein, Caroline Z. Wang, Shabarinath Srikumar, Scott Nguyen, Athmanya Eshwar, Roger Stephan, Angelika Lehner, Séamus Fanning, Ben D. Tall, Gopal R. Gopinath

Research output: Contribution to journal › Review article › peer-review

15 Citations (Scopus)

Abstract

Microorganisms express various transmembrane complexes collectively known as efflux pumps that influence their survival under stressful growth conditions. Although efflux pumps are important in resistance to antibiotics, disinfectants, and preservatives, little information about their presence and roles in Cronobacter spp. is available. To better understand the phylogeny, prevalence, and distribution of efflux pumps among strains of Cronobacter spp., whole genome sequencing (WGS) and pan-genomic DNA microarray (MA) analysis were carried out. Targeted MA analysis with 156 probe set alleles representing efflux pump genetic loci showed that all seven Cronobacter species possessed species-specific efflux pump orthologues. Distribution of the efflux pump genes and sequence variations were studied using WGS datasets. Phylogenetic and molecular clock analyses showed that the acquisition of these efflux pump genes possibly occurred at separate evolutionary events, which most likely correlated with the evolution of sequence type (ST) lineages. The acquisition of efflux pump genes either occurred as independent evolutionary events through horizontal gene transfer, or in certain situations, such as that for ST83 and ST4 strains, they could have been acquired through a robust microevolutionary selective process, some of which may have provided functional advantages. Efflux pump activity is very important in osmotic adaptation, survival, and persistence of Cronobacter species and are involved in several important physiological processes including protein, heavy metal, and sugar efflux. Understanding the mechanisms of Cronobacter adaptation in a wide range of environments, could eventually lead to development of methods to control the contamination of foods by these organisms.

Original language	English
Pages (from-to)	32-42
Number of pages	11
Journal	Current Opinion in Food Science
Volume	30
Early online date	20 Dec 2018
DOIs	https://doi.org/10.1016/j.cofs.2018.11.005
Publication status	Published - Dec 2019
Externally published	Yes

Bibliographical note

Funding Information:
We thank the student internship programs sponsored by the Office of International Affairs of Gachon University , Seongnam-si, Republic of Korea for supporting student interns: Jungha Woo and Youyoung Lee. We thank the University of Maryland at College Park, Joint Institute for Food Safety and Applied Nutrition (JIFSAN) for supporting JIFSAN interns Samantha Finkelstein and Flavia Negrete. We also thank the Oak Ridge Institute for Science and Education of Oak Ridge, Tennessee for sponsoring research fellows Hannah R. Chase and Hyein Jang. We thank the FDA ’s Pathways program for supporting Caroline Z. Wang. Funds sponsoring this work were obtained internally through U.S. FDA appropriations and this research was also funded in part by the University of Maryland JIFSAN Program through a cooperative agreement with the FDA, #FDU001418.

Funding Information:
We thank the student internship programs sponsored by the Office of International Affairs of Gachon University, Seongnam-si, Republic of Korea for supporting student interns: Jungha Woo and Youyoung Lee. We thank the University of Maryland at College Park, Joint Institute for Food Safety and Applied Nutrition (JIFSAN) for supporting JIFSAN interns Samantha Finkelstein and Flavia Negrete. We also thank the Oak Ridge Institute for Science and Education of Oak Ridge, Tennessee for sponsoring research fellows Hannah R. Chase and Hyein Jang. We thank the FDA's Pathways program for supporting Caroline Z. Wang. Funds sponsoring this work were obtained internally through U.S. FDA appropriations and this research was also funded in part by the University of Maryland JIFSAN Program through a cooperative agreement with the FDA, #FDU001418.

Publisher Copyright:
© 2018 Elsevier Ltd

ASJC Scopus subject areas

Food Science
Applied Microbiology and Biotechnology

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Cite this

Negrete, F., Jang, H., Gangiredla, J., Woo, J. H., Lee, Y. Y., Patel, I. R., Chase, H. R., Finkelstein, S., Wang, C. Z., Srikumar, S., Nguyen, S., Eshwar, A., Stephan, R., Lehner, A., Fanning, S., Tall, B. D., & Gopinath, G. R. (2019). Genome-wide survey of efflux pump-coding genes associated with Cronobacter survival, osmotic adaptation, and persistence. Current Opinion in Food Science, 30, 32-42. https://doi.org/10.1016/j.cofs.2018.11.005

@article{ecfb970963564ea0997ca22a967a51b6,

title = "Genome-wide survey of efflux pump-coding genes associated with Cronobacter survival, osmotic adaptation, and persistence",

abstract = "Microorganisms express various transmembrane complexes collectively known as efflux pumps that influence their survival under stressful growth conditions. Although efflux pumps are important in resistance to antibiotics, disinfectants, and preservatives, little information about their presence and roles in Cronobacter spp. is available. To better understand the phylogeny, prevalence, and distribution of efflux pumps among strains of Cronobacter spp., whole genome sequencing (WGS) and pan-genomic DNA microarray (MA) analysis were carried out. Targeted MA analysis with 156 probe set alleles representing efflux pump genetic loci showed that all seven Cronobacter species possessed species-specific efflux pump orthologues. Distribution of the efflux pump genes and sequence variations were studied using WGS datasets. Phylogenetic and molecular clock analyses showed that the acquisition of these efflux pump genes possibly occurred at separate evolutionary events, which most likely correlated with the evolution of sequence type (ST) lineages. The acquisition of efflux pump genes either occurred as independent evolutionary events through horizontal gene transfer, or in certain situations, such as that for ST83 and ST4 strains, they could have been acquired through a robust microevolutionary selective process, some of which may have provided functional advantages. Efflux pump activity is very important in osmotic adaptation, survival, and persistence of Cronobacter species and are involved in several important physiological processes including protein, heavy metal, and sugar efflux. Understanding the mechanisms of Cronobacter adaptation in a wide range of environments, could eventually lead to development of methods to control the contamination of foods by these organisms.",

author = "Flavia Negrete and Hyein Jang and Jayanthi Gangiredla and Woo, {Jung Ha} and Lee, {You Young} and Patel, {Isha R.} and Chase, {Hannah R.} and Samantha Finkelstein and Wang, {Caroline Z.} and Shabarinath Srikumar and Scott Nguyen and Athmanya Eshwar and Roger Stephan and Angelika Lehner and S{\'e}amus Fanning and Tall, {Ben D.} and Gopinath, {Gopal R.}",

note = "Funding Information: We thank the student internship programs sponsored by the Office of International Affairs of Gachon University , Seongnam-si, Republic of Korea for supporting student interns: Jungha Woo and Youyoung Lee. We thank the University of Maryland at College Park, Joint Institute for Food Safety and Applied Nutrition (JIFSAN) for supporting JIFSAN interns Samantha Finkelstein and Flavia Negrete. We also thank the Oak Ridge Institute for Science and Education of Oak Ridge, Tennessee for sponsoring research fellows Hannah R. Chase and Hyein Jang. We thank the FDA {\textquoteright}s Pathways program for supporting Caroline Z. Wang. Funds sponsoring this work were obtained internally through U.S. FDA appropriations and this research was also funded in part by the University of Maryland JIFSAN Program through a cooperative agreement with the FDA, #FDU001418. Funding Information: We thank the student internship programs sponsored by the Office of International Affairs of Gachon University, Seongnam-si, Republic of Korea for supporting student interns: Jungha Woo and Youyoung Lee. We thank the University of Maryland at College Park, Joint Institute for Food Safety and Applied Nutrition (JIFSAN) for supporting JIFSAN interns Samantha Finkelstein and Flavia Negrete. We also thank the Oak Ridge Institute for Science and Education of Oak Ridge, Tennessee for sponsoring research fellows Hannah R. Chase and Hyein Jang. We thank the FDA's Pathways program for supporting Caroline Z. Wang. Funds sponsoring this work were obtained internally through U.S. FDA appropriations and this research was also funded in part by the University of Maryland JIFSAN Program through a cooperative agreement with the FDA, #FDU001418. Publisher Copyright: {\textcopyright} 2018 Elsevier Ltd",

year = "2019",

month = dec,

doi = "10.1016/j.cofs.2018.11.005",

language = "English",

volume = "30",

pages = "32--42",

journal = "Current Opinion in Food Science",

issn = "2214-7993",

publisher = "Elsevier Ltd",

}

Negrete, F, Jang, H, Gangiredla, J, Woo, JH, Lee, YY, Patel, IR, Chase, HR, Finkelstein, S, Wang, CZ, Srikumar, S, Nguyen, S, Eshwar, A, Stephan, R, Lehner, A, Fanning, S, Tall, BD & Gopinath, GR 2019, 'Genome-wide survey of efflux pump-coding genes associated with Cronobacter survival, osmotic adaptation, and persistence', Current Opinion in Food Science, vol. 30, pp. 32-42. https://doi.org/10.1016/j.cofs.2018.11.005

TY - JOUR

T1 - Genome-wide survey of efflux pump-coding genes associated with Cronobacter survival, osmotic adaptation, and persistence

AU - Negrete, Flavia

AU - Jang, Hyein

AU - Gangiredla, Jayanthi

AU - Woo, Jung Ha

AU - Lee, You Young

AU - Patel, Isha R.

AU - Chase, Hannah R.

AU - Finkelstein, Samantha

AU - Wang, Caroline Z.

AU - Srikumar, Shabarinath

AU - Nguyen, Scott

AU - Eshwar, Athmanya

AU - Stephan, Roger

AU - Lehner, Angelika

AU - Fanning, Séamus

AU - Tall, Ben D.

AU - Gopinath, Gopal R.

N1 - Funding Information: We thank the student internship programs sponsored by the Office of International Affairs of Gachon University , Seongnam-si, Republic of Korea for supporting student interns: Jungha Woo and Youyoung Lee. We thank the University of Maryland at College Park, Joint Institute for Food Safety and Applied Nutrition (JIFSAN) for supporting JIFSAN interns Samantha Finkelstein and Flavia Negrete. We also thank the Oak Ridge Institute for Science and Education of Oak Ridge, Tennessee for sponsoring research fellows Hannah R. Chase and Hyein Jang. We thank the FDA ’s Pathways program for supporting Caroline Z. Wang. Funds sponsoring this work were obtained internally through U.S. FDA appropriations and this research was also funded in part by the University of Maryland JIFSAN Program through a cooperative agreement with the FDA, #FDU001418. Funding Information: We thank the student internship programs sponsored by the Office of International Affairs of Gachon University, Seongnam-si, Republic of Korea for supporting student interns: Jungha Woo and Youyoung Lee. We thank the University of Maryland at College Park, Joint Institute for Food Safety and Applied Nutrition (JIFSAN) for supporting JIFSAN interns Samantha Finkelstein and Flavia Negrete. We also thank the Oak Ridge Institute for Science and Education of Oak Ridge, Tennessee for sponsoring research fellows Hannah R. Chase and Hyein Jang. We thank the FDA's Pathways program for supporting Caroline Z. Wang. Funds sponsoring this work were obtained internally through U.S. FDA appropriations and this research was also funded in part by the University of Maryland JIFSAN Program through a cooperative agreement with the FDA, #FDU001418. Publisher Copyright: © 2018 Elsevier Ltd

PY - 2019/12

Y1 - 2019/12

N2 - Microorganisms express various transmembrane complexes collectively known as efflux pumps that influence their survival under stressful growth conditions. Although efflux pumps are important in resistance to antibiotics, disinfectants, and preservatives, little information about their presence and roles in Cronobacter spp. is available. To better understand the phylogeny, prevalence, and distribution of efflux pumps among strains of Cronobacter spp., whole genome sequencing (WGS) and pan-genomic DNA microarray (MA) analysis were carried out. Targeted MA analysis with 156 probe set alleles representing efflux pump genetic loci showed that all seven Cronobacter species possessed species-specific efflux pump orthologues. Distribution of the efflux pump genes and sequence variations were studied using WGS datasets. Phylogenetic and molecular clock analyses showed that the acquisition of these efflux pump genes possibly occurred at separate evolutionary events, which most likely correlated with the evolution of sequence type (ST) lineages. The acquisition of efflux pump genes either occurred as independent evolutionary events through horizontal gene transfer, or in certain situations, such as that for ST83 and ST4 strains, they could have been acquired through a robust microevolutionary selective process, some of which may have provided functional advantages. Efflux pump activity is very important in osmotic adaptation, survival, and persistence of Cronobacter species and are involved in several important physiological processes including protein, heavy metal, and sugar efflux. Understanding the mechanisms of Cronobacter adaptation in a wide range of environments, could eventually lead to development of methods to control the contamination of foods by these organisms.

AB - Microorganisms express various transmembrane complexes collectively known as efflux pumps that influence their survival under stressful growth conditions. Although efflux pumps are important in resistance to antibiotics, disinfectants, and preservatives, little information about their presence and roles in Cronobacter spp. is available. To better understand the phylogeny, prevalence, and distribution of efflux pumps among strains of Cronobacter spp., whole genome sequencing (WGS) and pan-genomic DNA microarray (MA) analysis were carried out. Targeted MA analysis with 156 probe set alleles representing efflux pump genetic loci showed that all seven Cronobacter species possessed species-specific efflux pump orthologues. Distribution of the efflux pump genes and sequence variations were studied using WGS datasets. Phylogenetic and molecular clock analyses showed that the acquisition of these efflux pump genes possibly occurred at separate evolutionary events, which most likely correlated with the evolution of sequence type (ST) lineages. The acquisition of efflux pump genes either occurred as independent evolutionary events through horizontal gene transfer, or in certain situations, such as that for ST83 and ST4 strains, they could have been acquired through a robust microevolutionary selective process, some of which may have provided functional advantages. Efflux pump activity is very important in osmotic adaptation, survival, and persistence of Cronobacter species and are involved in several important physiological processes including protein, heavy metal, and sugar efflux. Understanding the mechanisms of Cronobacter adaptation in a wide range of environments, could eventually lead to development of methods to control the contamination of foods by these organisms.

U2 - 10.1016/j.cofs.2018.11.005

DO - 10.1016/j.cofs.2018.11.005

M3 - Review article

AN - SCOPUS:85058624780

SN - 2214-7993

VL - 30

SP - 32

EP - 42

JO - Current Opinion in Food Science

JF - Current Opinion in Food Science

ER -

Genome-wide survey of efflux pump-coding genes associated with Cronobacter survival, osmotic adaptation, and persistence

Abstract

Bibliographical note

ASJC Scopus subject areas

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