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Stress and microbial endocrinology: prospects for ruminant nutrition

Published online by Cambridge University Press:  23 April 2010

P. Freestone  and
M. Lyte
P. Freestone*
Affiliation:
Department of Infection, Immunity and Inflammation, University of Leicester, Leicester, LE1 9HN, UK
M. Lyte
Affiliation:
Department of Pharmacy Practice, School of Pharmacy, Texas Tech University Health Sciences Center, Lubbock, TX 79430, USA
*
†E-mail: ppef1@le.ac.uk
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Abstract

The feed efficiency of ruminant meat and dairy livestock can be significantly influenced by factors within their living environments. In particular, events perceived by the animals as stressful (such as parturition, transport or handling) have been found to affect susceptibility to infection. It has been well documented that even minor stress such as weighing can result in an increase in colonisation and faecal shedding of enteric pathogens such as Salmonella enterica and Escherichia coli O157:H7. Such infections affect both ruminant overall health and therefore performance, and are a particular problem for the meat production industries. Prior explanations for stress enhancing the likelihood of infection is that activation of the sympathetic nervous system under stress leads to the release of neuroendocrine mediators such as the catecholamine stress hormones noradrenaline and adrenaline, which may impair innate and adaptive immunity. More recently, however, another equally compelling explanation, viewed through the lens of the newly recognised microbiological discipline of microbial endocrinology is that the myriad of bacteria within the ruminant digestive tract are as responsive to the hormonal output of stress as the cells of their host. Work from our laboratories has shown that enteric pathogens have evolved systems for directly sensing stress hormones. We have demonstrated that even brief exposure of enteric pathogens to physiological concentrations of stress hormones can result in massive increases in growth and marked changes in expression of virulence factors such as adhesins and toxins. Happy, less stressed ruminants may therefore be better-nourished animals and safer sources of meat. This article reviews evidence that stress, as well as affecting nutrition, in ruminants is correlated with increased risk of enteric bacterial infections, and examines the molecular mechanisms that may be at work in both processes.

Keywords

microbial endocrinologystressruminantinfection
Type
Full Paper
Information
animal , Volume 4 , Issue 7: XIth International Symposium on Ruminant Physiology (ISRP), 6–9 September, 2009 Clermont-Ferrand (France) , July 2010 , pp. 1248 - 1257
Copyright
Copyright © The Animal Consortium 2010

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References

Alverdy, J, Holbrook, C, Rocha, F, Seiden, L, Wu, RL, Musch, M, Chang, E, Ohman, D, Suh, S 2000. Gut-derived sepsis occurs when the right pathogen with the right virulence genes meets the right host: evidence for in vivo virulence expression in Pseudomonas aeruginosa. Annals of Surgery 232, 480–489.CrossRefGoogle ScholarPubMed
Anderson, M, Armstrong, SK 2006. The Bordetella Bfe system: growth and transcriptional response to siderophores, catechols, and neuroendocrine catecholamines. Journal of Bacteriology 188, 5731–5740.CrossRefGoogle ScholarPubMed
Anderson, M, Armstrong, SK 2008. Norepinephrine mediates acquisition of transferring-iron in Bordetella bronchiseptica. Journal of Bacteriology 190, 3940–3947.CrossRefGoogle Scholar
Bailey, MT, Engler, H, Sheridan, JF 2006. Stress induces the translocation of cutaneous and gastrointestinal microflora to secondary lymphoid organs of C57BL/6 mice. Journal of Neuroimmunology 171, 29–37.CrossRefGoogle ScholarPubMed
Bailey, MT, Dowd, SE, Parry, NM, Galley, JD, Schauer, DB, Lyte, M 2010. Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infection and Immunity [Epub ahead of print]. PMID: 20145094.CrossRefGoogle ScholarPubMed
Bansal, T, Englert, D, Lee, J, Hegde, M, Wood, TK, Jayaraman, A 2007. Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization and gene expression. Infection and Immunity 75, 4597–4607.CrossRefGoogle ScholarPubMed
Belay, T, Aviles, H, Vance, M, Fountain, K, Sonnenfeld, G 2003. Catecholamines and in vitro growth of pathogenic bacteria: enhancement of growth varies greatly among bacterial species. Life Sciences 73, 1527–1535.CrossRefGoogle ScholarPubMed
Boissy, A, Manteuffel, G, Jensen, MB, Moe, RO, Sprujit, B, Keeling, LJ, Winckler, C, Forkamn, B, Dimitrov, I, Lagbein, J, Bakken, M, Veissier, I, Aubert, A 2007. Assessment of positive emotions in animals to improve their welfare. Physiology and Behaviour 92, 375–397.CrossRefGoogle ScholarPubMed
Chen, C, Brown, DR, Xie, Y, Green, BT, Lyte, M 2003. Catecholamines modulate Escherichia coli O157:H7 adherence to murine cecal mucosa. Shock 20, 183–188.CrossRefGoogle ScholarPubMed
Chen, C, Lyte, M, Stevens, MP, Vulchanova, L, Brown, DR 2006. Mucosally directed adrenergic nerves and sympathomimetric drugs enhance non-intimate adherence of Escherichia coli O157:H7 to porcine cecum and colon. European Journal Pharmacology 539, 116–124.CrossRefGoogle Scholar
Cogan, TA, Thomas, AO, Rees, LE, Taylor, AH, Jepson, MA, Williams, PH, Ketley, J, Humphrey, TJ 2007. Norepinephrine increases the pathogenic potential of Campylobacter jejuni. Gut 56, 1060–1065.CrossRefGoogle ScholarPubMed
Coulanges, V, Andre, P, Vidon, DJ 1997. Effect of siderophores, catecholamines, and catechol compounds on Listeria spp. growth in iron-complexed medium. Biochemical Biophysical Research Communications 249, 526–530.CrossRefGoogle Scholar
Dowd, SE 2007. Escherichia coli O157:H7 gene expression in the presence of catecholamine norepinephrine. FEMS Microbiology Letters 273, 214–223.CrossRefGoogle ScholarPubMed
Dowd, SE, Callaway, TR, Morrow-Tesch, J 2007. Handling may cause increased shedding of Escherichia coli and total coliforms in pigs. Foodborne Pathogenic Diseases 4, 99–102.CrossRefGoogle ScholarPubMed
Dréau, D, Sonnenfeld, G, Fowler, N, Morton, DS, Lyte, M 1999. Effects of social conflict on immune responses and E. coli growth within closed chambers in mice. Physiology and Behavior 67, 133–140.CrossRefGoogle Scholar
Eisenhofer, G, Aneman, A, Friberg, P, Hooper D Fåndriks, L, Lonroth, H, Hunyady, B, Mezey, E 1997. Substantial production of dopamine in the human gastrointestinal tract. Journal of Clinical Endocrinology and Metabolism 82, 3864–3871.CrossRefGoogle ScholarPubMed
Freestone, PP, Haigh, RD, Lyte, M 2007a. Specificity of catecholamine-induced growth in Escherichia coli O157:H7, Salmonella enterica and Yersinia enterocolitica. FEMS Microbiology Letters 269, 221–228.CrossRefGoogle ScholarPubMed
Freestone, PP, Lyte, M, Haigh, RD, Williams, PH 1999. Stimulation of bacterial growth by heat-stable norepinephrine-induced autoinducers. FEMS Microbiology Letters 172, 53–60.CrossRefGoogle ScholarPubMed
Freestone, PP, Haigh, RD, Williams, PH, Lyte, M 2003. Involvement of enterobactin in norepinephrine-mediated iron supply from transferrin to enterohaemorrhagic Escherichia coli. FEMS Microbiology Letters 222, 39–43.CrossRefGoogle ScholarPubMed
Freestone, PP, Walton, NJ, Haigh, RD, Lyte, M 2007b. Influence of dietary catechols on the growth of enteropathogenic bacteria. International Journal of Food Microbiology 119, 159–169.CrossRefGoogle ScholarPubMed
Freestone, PP, Sandrini, SM, Haigh, RD, Lyte, M 2008. Microbial endocrinology: how stress influences susceptibility to infection. Trends in Microbiology 16, 55–64.CrossRefGoogle ScholarPubMed
Freestone, PP, Lyte, M, Neal, CP, Maggs, AF, Haigh, RD, Williams, PH 2000. The mammalian neuroendocrine hormone norepinephrine supplies iron for bacterial growth in the presence of transferrin or lactoferrin. Journal of Bacteriology 182, 6091–6098.CrossRefGoogle ScholarPubMed
Freestone, PP, Williams, PH, Haigh, RD, Maggs, AF, Neal, CP, Lyte, M 2002. Growth stimulation of intestinal commensal Escherichia coli by catecholamines: a possible contributory factor in trauma-induced sepsis. Shock 18, 465–470.CrossRefGoogle ScholarPubMed
Furness, JB 2006. The Enteric Nervous System. Blackwell Publishers, Oxford, UK.Google Scholar
Green, BT, Lyte, M, Kulkarni-Narla, A, Brown, DR 2003. Neuromodulation of enteropathogen internalization in Peyer’s patches from porcine jejunum. Journal of Neuroimmunology 141, 74–82.CrossRefGoogle ScholarPubMed
Green, BT, Lyte, M, Chen, C, Xie, Y, Casey, MA, Kulkarni-Narla, A, Vulchanova, L, Brown, DR 2004. Adrenergic modulation of Escherichia coli O157:H7 adherence to the colonic mucosa. American Journal of Physiology – Gastrointestinal Liver Physiology 287, G1238–G1246.CrossRefGoogle Scholar
Hemsworth, PH 2003. Human-animal interactions in live stock production. Applied Animal Behaviour Science 81, 185–198.CrossRefGoogle Scholar
Hemsworth, PH, Barnett, JL, Tilbrook, AJ, Hansen, C 1998. The effects of handling by humans at calving and during milking on the behaviour and milk cortisol concentrations of primiparous dairy cows. Applied Animal Behaviour Science 22, 313–336.CrossRefGoogle Scholar
Hendrickson, BA, Guo, J, Laughlin, R, Chen, Y, Alverdy, JC 1999. Increased type 1 fimbrial expression among commensal Escherichia coli isolates in the murine cecum following catabolic stress. Infection and Immunity 67, 745–753.CrossRefGoogle ScholarPubMed
Herskin, MS, Munksgaard, L, Ladewig, J 2004. Effects of acute stressors on nociception, adrenocortical responses and behaviour of dairy cows. Physiology and Behaviour 93, 411–420.CrossRefGoogle Scholar
Kinney, KS, Austin, CE, Morton, DS, Sonnenfeld, G 1999. Catecholamine enhancement of Aeromonas hydrophila growth. Microbial Pathogenesis 26, 85–91.CrossRefGoogle ScholarPubMed
Kendall, MM, Rasko, DA, Sperandio, V 2007. Global effects of the cell-to-cell signaling molecules autoinducer-2, autoinducer-3, and epinephrine in a luxS mutant of enterohemorrhagic Escherichia coli. Infection and Immunity 7, 4875–4884.CrossRefGoogle Scholar
Lacoste, A, Jalabert, F, Malham, SK, Cueff, A, Poulet, SA 2001. Stress and stress-induced neuroendocrine changes increase the susceptibility of juvenile oysters (Crassostrea gigas) to Vibrio splendidus. Applied and Environmental Microbiology 67, 2304–2309.CrossRefGoogle ScholarPubMed
Lenz, HJ, Raedler, A, Greten, H, Vale, WW, Rivier, JE 1988. Stress-induced gastrointestinal secretory and motor responses in rats are mediated by endogenous corticotropin-releasing factor. Gastroenterology 95, 1510–1517.CrossRefGoogle ScholarPubMed
Lyte, M 1993. The role of microbial endocrinology in infectious disease. Journal of Endocrinology 137, 343–345.CrossRefGoogle ScholarPubMed
Lyte, M 2004a. Microbial endocrinology and infectious disease in the 21st century. Trends in Microbiology 12, 14–20.CrossRefGoogle Scholar
Lyte, M 2004b. The biogenic amine tyramine modulates the adherence of Escherichia coli O157:H7 to intestinal mucosa. Journal of Food Protection 67, 878–883.CrossRefGoogle ScholarPubMed
Lyte, M, Ernst, S 1992. Catecholamine induced growth of gram negative bacteria. Life Sciences 50, 203–212.CrossRefGoogle ScholarPubMed
Lyte, M, Bailey, MT 1997. Neuroendocrine-bacterial interactions in a neurotoxin-induced model of trauma. Journal of Surgical Research 70, 195–201.CrossRefGoogle Scholar
Lyte, M, Frank, CD, Green, BT 1996a. Production of an autoinducer of growth by norepinephrine cultured Escherichia coli O157:H7. FEMS Microbiology Letters 139, 155–159.CrossRefGoogle ScholarPubMed
Lyte, M, Arulanandam, BP, Frank, CD 1996b. Production of Shiga-like toxins by Escherichia coli O157:H7 can be influenced by the neuroendocrine hormone norepinephrine. Journal of Laboratory & Clinical Medicine 128, 392–398.CrossRefGoogle ScholarPubMed
Lyte, M, Arulanandam, B, Nguyen, K, Frank, C, Erickson, A, Francis, D 1997. Norepinephrine induced growth and expression of virulence associated factors in enterotoxigenic and enterohemorrhagic strains of Escherichia coli. Advances in Experimental Medicine and Biology 412, 331–339.CrossRefGoogle ScholarPubMed
Lyte, M, Freestone, PP, Neal, CP, Olson, BA, Haigh, RD, Bayston, R, Williams, PH 2003. Stimulation of Staphylococcus epidermidis growth and biofilm formation by catecholamine inotropes. Lancet 361, 130–135.CrossRefGoogle ScholarPubMed
Mishra, SK, Segal, E, Gunter, E, Kurup, VP, Mishra, J, Murali, PS, Pierson, DL, Sandovsky-Losica, H, Stevens, DA 1994. Stress, immunity and mycotic diseases. Journal of Medical and Veterinary Mycology 32 (suppl. 1), 379–406.CrossRefGoogle ScholarPubMed
Munskgaard, L, De Passille, AM, Rushen, J, Herskin, MS, Kristensen, AM 2001. Dairy cows fear of people: social learning, milk yield and behaviour at milking. Applied Animal Behaviour Science 73, 15–26.CrossRefGoogle Scholar
Nakade, Y, Tsuchida, D, Fukuda, H, Iwa, M, Pappas, TN, Takahashi, T 2005. Restraint stress delays solid gastric emptying via a central CRF and peripheral sympathetic neuron in rats. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 288, R427–R432.CrossRefGoogle Scholar
Nakano, M, Takahashi, A, Sakai, Y, Nakaya, Y 2007b. Modulation of pathogenicity with norepinephrine related to the type III secretion system of Vibrio parahaemolyticus. Journal of Infectious Diseases 195, 1353–1360.CrossRefGoogle Scholar
Nakano, M, Takahashi, A, Sakai, Y, Kawano, M, Harada, N, Mawatari, K, Nakaya, Y 2007a. Catecholamine-induced stimulation of growth in Vibrio species. Letters in Applied Microbiology 44, 649–653.CrossRefGoogle ScholarPubMed
Neal, CP, Freestone, PP, Maggs, AF, Haigh, RD, Williams, PH, Lyte, M 2001. Catecholamine inotropes as growth factors for Staphylococcus epidermidis and other coagulase-negative staphylococci. FEMS Microbiology Letters 194, 163–169.CrossRefGoogle ScholarPubMed
Nieuwenhuijzen, GA, Deitch, EA, Goria, RJ 1996. Infection, the gut and the development of multiple organ dysfunction syndrome. European Journal of Surgery 162, 259–273.Google ScholarPubMed
O’Donnell, PM, Aviles, H, Lyte, M, Sonnenfeld, G 2006. Enhancement of in vitro growth of pathogenic bacteria by norepinephrine: importance of inoculum density and role of transferrin. Applied and Environmental Microbiology 72, 5097–5099.CrossRefGoogle ScholarPubMed
O’Neal, MJ, Schafer, ER, Madsen, ML, Minion, FC 2008. Global transcriptional analysis of Mycoplasma hyponeumoniae following exposure to norepinephrine. Microbiology 154, 2581–2588.CrossRefGoogle Scholar
Ratledge, C, Dover, LG 2000. Iron metabolism in pathogenic bacteria. Annual Review of Microbiology 54, 881–941.CrossRefGoogle ScholarPubMed
Reiche, EM, Nunes, SO, Morimoto, HK 2004. Stress, depression, the immune system, and cancer. The Lancet Oncology 5, 617–625.CrossRefGoogle ScholarPubMed
Reissbrodt, R, Rienaecker, I, Romanova, JM, Freestone, PP, Haigh, RD, Lyte, M, Tschäpe, H, Williams, PH 2002. Resuscitation of Salmonella enterica serovar typhimurium and enterohemorrhagic Escherichia coli from the viable but nonculturable state by heat-stable enterobacterial autoinducer. Applied and Environmental Microbology 68, 4788–4794.CrossRefGoogle ScholarPubMed
Roberts, A, Matthews, J, Socransky, S, Freestone, P, Williams, P, Chapple, I 2002. Stress and the periodontal diseases: effects of catecholamines on the growth of periodontal bacteria in vitro. Oral Microbiology and Immunology 17, 296–303.CrossRefGoogle ScholarPubMed
Roberts, A, Matthews, J, Socransky, S, Freestone, P, Williams, P, Chapple, I 2005. Stress and the periodontal diseases: growth responses of periodontal bacteria to Escherichia coli stress-associated autoinducer and exogenous Fe. Oral Microbiology and Immunology 20, 147–153.CrossRefGoogle ScholarPubMed
Scheckelhoff, MR, Telford, SR, Wesley, M, Hu, LT 2007. Borrelia burgdorferi intercepts host hormonal signals to regulate expression of outer surface protein A. Proceedings National Academy of Sciences USA 104, 7247–7252.CrossRefGoogle ScholarPubMed
Schreiber, KL, Brown, DR 2005. Adrenocorticotrophic hormone modulates Escherichia coli O157:H7 adherence to porcine colonic mucosa. Stress 8, 185–190.CrossRefGoogle ScholarPubMed
Sperandio, V, Torres, AG, Jarvis, B, Nataro, JP, Kaper, J 2003. Bacteria-host communication: the language of hormones. Proceedings National Academy of Sciences USA 100, 8951–8956.CrossRefGoogle ScholarPubMed
Tajima, K, Nonaka, I, Higuchi, K, Takasuri, N, Kurihara, H, Takenaka, A, Mitsumori, M, Kajikawa, H, Aminov, R 2007. Influence of high temperature and humidity on rumen bacterial diversity in Holstein heifers. Anaerobe 13, 57–64.CrossRefGoogle ScholarPubMed
Tamminga, S, Schrama, JW 1998. Environmental effects on nutrient and energy metabolism in ruminants. Archives of Animal Nutrition 51, 2225–2235.Google ScholarPubMed
Tarr, PI, Neill, MA 2001. Escherichia coli O157:H7. Gastroenterology Clinic North America 30, 735–751.CrossRefGoogle ScholarPubMed
Terlouw, EM, Arnould, C, Auperin, B, Berri, C, Le Bihan-Duval, E, Deiss, V, Lefevre, F, Lenskink, BJ, Mounier, L 2008. Pre-slaughter conditions, animal stress and welfare: current status and possible future research. Animal 2, 1501–1517.CrossRefGoogle ScholarPubMed
Toscano, MJ, Stabel, TJ, Bearson, SM, Bearson, BL, Lay, DC Jr 2007. Cultivation of Salmonella enterica serovar typhimurium in a norepinephrine-containing medium alters in vivo tissue prevalence in swine. Journal Experimental Animal Science 43, 329–338.CrossRefGoogle Scholar
Uyeno, Y, Sekiguchi, Y, Tajima, K, Takenaka, A, Kurihara, M 2010. An rRNA analysis for evaluating the effect of heat stress on the rumen microbial composition of Holstein heifers. Anaerobe 16, 27–33.CrossRefGoogle ScholarPubMed
Vlisidou, I, Lyte, M, Van Diemen, PM, Hawes, P, Monaghan, P, Wallis, TS, Stevens, MP 2004. The neuroendocrine stress hormone norepinephrine augments Escherichia coli O157:H7-induced enteritis and adherence in a bovine ligated ileal loop model of infection. Infection and Immunity 72, 5446–5451.CrossRefGoogle Scholar
Voigt, W, Fruth, A, Tschape, H, Reissbrodt, R, Williams, PH 2006. Enterobacterial autoinducer of growth enhances shiga toxin production by enterohemorrhagic Escherichia coli. Journal of Clinical Microbiology 44, 2247–2249.CrossRefGoogle ScholarPubMed
Webster, J, Tonelli, L, Sternberg, E 2002. Neuroendocrine regulation of immunity. Annual Review of Immunology 20, 125–163.CrossRefGoogle ScholarPubMed
Williams, PH, Rabsch, W, Methner, U, Voigt, W, Tschäpe, H, Reissbrodt, R 2006. Catecholate receptor proteins in Salmonella enterica: role in virulence and implications for vaccine development. Vaccine 24, 840–3844.CrossRefGoogle ScholarPubMed
Zhou, M, Simms, H, Wang, P 2004. Increased gut-derived norepinephrine release in sepsis: up-regulation of intestinal tyrosine hydroxylase. Biochimica et Biophysica Acta 1689, 212–218.CrossRefGoogle ScholarPubMed