Av ian Salmonella enteritidis serovar Enteritidis with ClpP deletion is attenuated and highly immunogenic in chickens
Salmonella enterica subsp.
enterica
serovars are leading causative agents of gastroenteritis in humans and numerous animal
species worldwide. The
ClpP
from
Salmonella enterica
is responsible for regulation under various stress conditions. We were interested in
the effect of
ClpP
deletion mutation on attenuation of
Salmonella enterica
subsp.
enterica
serovar Enteritidis (SE) in chickens. Therefore,
SM-6/Δ
ClpP
, deletion of the
ClpP
gene from a wild-type SE-6 (SM-6) strain, was generated using the phage &lamda; Red homologous
recombination. Compared with SM-6, SM-6/&DeltaClpP
represented a retarded growth rate and lower concentration in LB broth with and
without 5% NaCl or lower pH values, indicating that it is sensitive to conventional disinfectants. SM-6/Δ
ClpP
represented reduced
invasion into macrophages in vitro and an approximate 400-fold attenuation based on cell invasion assay and median lethal dose (LD
50
)
in specific pathogen-free (SPF) chickens. Furthermore, SM-6/Δ
ClpP
showed reduced colonization in the liver and spleen and faster
clearance compared with SM-6, indicating a short discharge. The survival rate of 7-day-old SPF chickens immunized with SM-6/Δ
ClpP
against homologous challenge and antibody kinetics indicated that SM-6/ΔClpP
provided efficient protection from lethal challenge and
induced robust antibody immune responses, demonstrating the potential of live, attenuated SE
as a
vaccine candidate.
___
- Guo Z, Su C, Huang J, Niu J. A food-borne outbreak of
gastroenteritis caused by different Salmonella serotypes in 2
universities in Xiamen, Fujian, China, in 2012. Jpn J Infect Dis
2015; 68: 187-191.
- Lutful Kabir SM. Avian colibacillosis and salmonellosis: a
closer look at epidemiology, pathogenesis, diagnosis, control
and public health concerns. Int J Environ Res Public Health
2010; 7: 89-114.
- Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Gast
R, Humphrey TJ, Van Immerseel F. Mechanisms of egg
contamination by
Salmonella
Enteritidis. FEMS Microbiol Rev
2009; 33: 718-738.
- Van Doren JM, Neil KP, Parish M, Gieraltowski L, Gould LH,
Gombas KL. Foodborne illness outbreaks from microbial
contaminants in spices, 1973-2010. Food Microbiol 2013; 36:
456-464.
- Thompson Bastin ML, Neville NR, Parsons RE, Flannery
AH, Tennant SJ, Johnson CA. An unusual case of
Salmonella
Enteritidis causing pneumonia, septic shock and multiple
organ failure in an immunocompetent patient. IDCases 2016;
6: 85-89.
- Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM,
Jensen AB, Wegener HC, Aarestrup FM. Global monitoring
of
Salmonella
serovar distribution from the World Health
Organization Global Foodborne Infections Network Country
Data Bank: results of quality assured laboratories from 2001 to
2007. Foodborne Pathog Dis 2011; 8: 887-900.
- Morales-Barrera E, Calhoun N, Lobato-Tapia JL, Lucca V,
Prado-Rebolledo O, Hernandez-Velasco X, Merino-Guzman
R, Petrone-Garcia VM, Latorre JD, Mahaffey BD et al. Risks
involved in the use of enrofloxacin for
Salmonella
Enteritidis
or
Salmonella
Heidelberg in commercial poultry. Front Vet Sci
2016; 3: 72.
- Fernandez Marquez ML, Burgos MJ, Pulido RP, Galvez A,
Lopez RL. Biocide tolerance and antibiotic resistance in
Salmonella
isolates from hen eggshells. Foodborne Pathog Dis
2017; 14: 89-95.
- Bolan NS, Szogi AA, Chuasavathi T, Seshadri B, Rothrock
MJ, Panneerselvam P. Uses and management of poultry litter.
World’s Poultry Science Journal 2010; 66: 673-698.
- Cogan TA, Humphrey TJ. The rise and fall of
Salmonella
Enteritidis in the UK. J Appl Microbiol 2003; 94 (Suppl.):
114S-119S.
- MacLennan CA. Antibodies and protection against invasive
salmonella disease. Front Immunol 2014; 5: 635.
- Lillehoj EP, Yun CH, Lillehoj HS. Vaccines against the avian
enteropathogens
Eimeria
,
Cryptosporidium
and
Salmonella
.
Anim Health Res Rev 2000; 1: 47-65.
- Penha Filho RA, de Paiva JB, Arguello YM, da Silva MD,
Gardin Y, Resende F, Berchieri Junior AB, Sesti L. Efficacy
of several vaccination programmes in commercial layer and
broiler breeder hens against experimental challenge with
Salmonella enterica
serovar Enteritidis. Avian Pathol 2009; 38:
367-375.
- Foley SL, Nayak R, Hanning IB, Johnson TJ, Han J, Ricke
SC. Population dynamics of
Salmonella enterica
serotypes
in commercial egg and poultry production. Appl Environ
Microbiol 2011; 77: 4273-4279.
- Matulova M, Havlickova H, Sisak F, Babak V, Rychlik I.
SPI1 defective mutants of
Salmonella enterica
induce cross-
protective immunity in chickens against challenge with
serovars Typhimurium and Enteritidis. Vaccine 2013; 31: 3156-
3162.
- Figueira R, Watson KG, Holden DW, Helaine S. Identification
of salmonella pathogenicity island-2 type III secretion system
effectors involved in intramacrophage replication of
S. enterica
serovar typhimurium: implications for rational vaccine design.
MBio 2013; 4: e00065.
- Zhou Y, Zhou J, Wang D, Gao Q, Mu X, Gao S, Liu X. Evaluation
of ompA and pgtE genes in determining pathogenicity in
Salmonella enterica
serovar Enteritidis. Vet J 2016; 218: 19-26.
- Methner U, Barrow PA, Berndt A, Rychlik I.
Salmonella
Enteritidis with double deletion in phoPfliC--a potential live
Salmonella
vaccine candidate with novel characteristics for use
in chickens. Vaccine 2011; 29: 3248-3253.
- Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E, Holden
DW. Simultaneous identification of bacterial virulence genes
by negative selection. Science 1995; 269: 400-403.
- Matsui H, Suzuki M, Isshiki Y, Kodama C, Eguchi M, Kikuchi
Y, Motokawa K, Takaya A, Tomoyasu T, Yamamoto T. Oral
immunization with ATP-dependent protease-deficient mutants
protects mice against subsequent oral challenge with virulent
Salmonella enterica serovar typhimurium. Infect Immun 2003;
71: 30-39.
- Knudsen GM, Olsen JE, Aabo S, Barrow P, Rychlik I,
Thomsen LE. ClpP deletion causes attenuation of
Salmonella
Typhimurium virulence through mis-regulation of RpoS and
indirect control of CsrA and the SPI genes. Microbiology 2013;
159: 1497-1509.
- Tu J, Huang B, Zhang Y, Zhang Y, Xue T, Li S, Qi K. Modulation
of virulence genes by the two-component system PhoP-PhoQ
in avian pathogenic
Escherichia coli
. Pol J Vet Sci 2016; 19: 31-
40.
- Gerlach RG, Jackel D, Holzer SU, Hensel M. Rapid
oligonucleotide-based recombineering of the chromosome of
Salmonella enterica
. Appl Environ Microbiol 2009; 75: 1575-
1580.
- Si W, Wang X, Liu H, Yu S, Li Z, Chen L, Zhang W, Liu
S. Physiology, pathogenicity and immunogenicity of live,
attenuated
Salmonella enterica
serovar Enteritidis mutants in
chicks. Microb Pathog 2015; 83-84: 6-11.
- Datsenko KA, Wanner BL. One-step inactivation of
chromosomal genes in
Escherichia coli
K-12 using PCR
products. P Natl Acad Sci USA 2000; 97: 6640-6645.
- Gur E, Biran D, Ron EZ. Regulated proteolysis in Gram-
negative bacteria--how and when? Nat Rev Microbiol 2011; 9:
839-848.
- Thomsen LE, Olsen JE, Foster JW, Ingmer H. ClpP is involved
in the stress response and degradation of misfolded proteins in
Salmonella enterica
serovar Typhimurium. Microbiology 2002;
148: 2727-2733.