What is the Body Temperature of a Chicken? A Complete Guide to Poultry Thermoregulation

Bryan TroxellaPrestage Department of Poultry Science, North Carolina State University, Raleigh, North Carolina, USAFind articles by

Received 2015 Aug 12; Accepted 2015 Sep 15; Prepublished 2015 Sep 18; Issue date 2015 Dec. Copyright © 2015, American Society for Microbiology. All Rights Reserved.

Salmonella enterica serovars Typhimurium (S. Typhimurium) and Enteritidis (S. Enteritidis) are foodborne pathogens, and outbreaks are often associated with poultry products. Chickens are typically asymptomatic when colonized by these serovars; however, the factors contributing to this observation are uncharacterized. Whereas symptomatic mammals have a body temperature between 37°C and 39°C, chickens have a body temperature of 41°C to 42°C. Here, in vivo experiments using chicks demonstrated that numbers of viable S. Typhimurium or S. Enteritidis bacteria within the liver and spleen organ sites were ≥4 orders of magnitude lower than those within the ceca. When similar doses of S. Typhimurium or S. Enteritidis were given to C3H/HeN mice, the ratio of the intestinal concentration to the liver/spleen concentration was 1:1. In the avian host, this suggested poor survival within these tissues or a reduced capacity to traverse the host epithelial layer and reach liver/spleen sites or both. Salmonella pathogenicity island 1 (SPI-1) promotes localization to liver/spleen tissues through invasion of the epithelial cell layer. Following in vitro growth at 42°C, SPI-1 genes sipC, invF, and hilA and the SPI-1 rtsA activator were downregulated compared to expression at 37°C. Overexpression of the hilA activators fur, fliZ, and hilD was capable of inducing hilA-lacZ at 37°C but not at 42°C despite the presence of similar levels of protein at the two temperatures. In contrast, overexpression of either hilC or rtsA was capable of inducing hilA and sipC at 42°C. These data indicate that physiological parameters of the poultry host, such as body temperature, have a role in modulating expression of virulence.

Salmonella enterica serovars Typhimurium (S. Typhimurium) and Enteritidis (S. Enteritidis) are major causes of foodborne diseases worldwide. In the United States, S. Typhimurium and S. Enteritidis accounted for the majority of confirmed cases of Salmonella outbreaks between 1970 and 2011 (1). These two are nontyphoid Salmonella (NTS) serovars that are capable of causing disease signs in a variety of animals, which contrasts with typhoid fever serovars that exclusively infect humans. Numerous food products have been associated with Salmonella outbreaks and illnesses in humans; however, poultry products are frequently implicated in outbreaks associated with NTS (www.cdc.gov/Salmonella/outbreaks.html). In 2010, a major poultry-related outbreak occurred that involved S. Enteritidis infections across 11 states and resulted in the recall of 380 million eggs (2).

S. Typhimurium invades the host epithelial cell layer and migrates to liver and spleen tissue sites through the action of a type 3 secretion system (T3SS), encoded by Salmonella pathogenicity island 1 (SPI-1). SPI-1 is a DNA segment that is approximately 40 kb in size and encodes the structural components of the secretion system, secreted and chaperone proteins, and transcription factors that activate expression of the SPI-1 genes (3–5). Three regulators that are carried within SPI-1, hilA, hilC, and hilD, and rtsA, which is carried outside SPI-1, are critical activators of the island. Collectively, the protein products encoded by genes within SPI-1 promote uptake of the pathogen by nonphagocytic cells of the hosts epithelial cell layer (6–8). Oral infection with S. Typhimurium mutants lacking the entire pathogenicity island or with Δspi1 or ΔhilA mutants results in severely limited localization of the mutant to the spleen compared to wild-type strain results, but this difference is not observed when mice are inoculated through the intraperitoneal route (9). This supports the concept that SPI-1 plays an important role in traversing the intestinal epithelial layer.

Invasion of the host epithelial cell layer is a critical aspect of S. Typhimurium virulence (10). RtsA forms a complex regulatory network with HilC and HilD that ultimately activates expression of hilA, which activates components of SPI-1 (9, 11). Recently, several works have contributed to our understanding of the complex regulation of SPI-1 (12–14). In addition, the DNA binding sites of the HilD protein have been mapped and include several genes that are coregulated by HilC and RtsA (15), suggesting that reduced activation by one of the three activators may influence the activation of coregulated genes.

Although poultry are associated with Salmonella outbreaks, poultry are largely asymptomatic. In general, oral administration of S. Typhimurium or S. Enteritidis to poultry results in poor localization and colonization of systemic tissues such as the liver and spleen compared to bacterial concentration within the ceca (16–20). Although the reasons for these results are likely multifactorial, the 3 to 5°C difference in the body temperature of poultry (41°C to 42°C) compared to susceptible mammals (37°C to 39°C) may be a factor contributing to the lack of systemic localization by these serovars in poultry. Since both serovars are capable of reaching systemic tissues in other animals, we hypothesized that the body temperature of chickens exerts a regulatory effect that limits expression of SPI-1 and localization to systemic tissues.

Here, we show that S. Typhimurium or S. Enteritidis colonized the ceca of a commercial breed of chicks but localized poorly to the liver and spleen, suggesting a low level of invasion. These results contrasted with data from the murine host, which exhibited similar concentrations of S. Typhimurium or S. Enteritidis within the intestines, spleen, and liver. Therefore, the effect of temperature on the regulation of SPI-1 was evaluated in cells grown at 37°C versus 42°C. Following growth at 42°C, there was reduced expression of SPI-1 genes. Gene expression studies conducted at 42°C demonstrated reduced activation of the rtsA gene, which is directly activated by HilD (15), suggesting a reduction in the level of either HilD or HilD protein activity in response to growth at 42°C. To gain insight into the mechanism resulting in the inability to activate SPI-1 at 42°C, we utilized an inducible system to test the roles of Fur, FliZ, HilC, RtsA (STM14_5188), and HilD. Inducible expression of either HilC or RtsA protein, but not of Fur, FliZ, or HilD, was sufficient to activate hilA following growth at 42°C. As previously shown, the Lon protease inhibited activation of SPI-1; however, the lack of lon still resulted in the inability to activate SPI-1 following growth at 42°C. Our results supported the hypothesis that the body temperature of poultry caused a regulatory change in the expression of SPI-1 genes that likely contributed to the poor localization to the liver and spleen. Thus, the body temperature of poultry is a significant barrier to activation of SPI-1 and may contribute to diminished invasion of S. Typhimurium or S. Enteritidis in vivo.

Effect of 42°C on transcriptional activators of SPI-

To understand how growth at 42°C repressed SPI-1 genes, the promoters of the three AraC/XylS-type activators, hilC, rtsA, and hilD, were cloned into the multicopy, promoterless pSP417 lacZ shuttle vector (34). These constructs were transformed into strains NC1040 and BTNC0025, and expression of each reporter fusion was determined following growth at 37°C or 42°C. Importantly, these plasmid constructs do not disrupt the chromosomal copies of hilC, rtsA, or hilD, which avoids complications in the interpretation of the data when one of these activators is mutated (9, 35). The activity seen with the empty vector, PhilC, or the PhilD fusion was not significantly altered by growth at 42°C. However, the expression of the HilD-activated PrtsA-lacZ fusion was significantly reduced in both serovars (Fig. 3A; see also Fig. S1A in the supplemental material). Thus, growth at 42°C reduced transcriptional control of sipC, invF, hilA, and rtsA and suggested that the activation of SPI-1 was diminished at 42°C.

The promoters of the SPI-1 activators, hilC and rtsA, are differentially regulated by growth at 42°C. (A) The promoters of hilC, rtsA, and hilD were cloned into the pSP417 multicopy shuttle vector (empty vector) upstream of a promoterless lacZ gene. Bacteria were grown as described for Fig. 1B and diluted 1:50 into LB-MOPS medium with 1 mM glucose at pH 7.4 at 37°C or 42°C. β-Galactosidase activity was measured after overnight growth. Data are from 4 separate experiments, and a statistically significant result compared to activity at 37°C was determined. The strains used were BTNC0002 to BTNC0005. (B) Bacteria were grown in LB-MOPS medium with 1 mM glucose at pH 7.4 at 37°C or 42°C. Total RNA was extracted at an OD600 of ∼1. cDNA was generated using gene-specific primers, and expression data were normalized to the rrsA 16S rRNA gene.

Expression data from lacZ fusions were confirmed in strains NC1040 and BTNC0025 by measuring mRNA levels of hilC, rtsA, and hilD. Bacteria were grown to an OD600 of ∼1 at 37°C or 42°C, and RNA was extracted for qRT-PCR. As with the lacZ data, expression of hilD was not influenced by growth at 42°C; however, expression of rtsA was reduced ∼9-fold (Fig. 3B). Although β-galactosidase levels from the pPhilC-lacZ construct approached statistical significance under conditions of growth at 42°C, the expression of hilC was not reduced (Fig. 3B). With strain BTNC0025, expression of rtsA was reduced >5-fold following growth at 42°C (see Fig. S1 in the supplemental material). Considering the results from both serovars, the data supported the conclusion that growth at 42°C reduced expression of the rtsA gene.

Previous work from our laboratory and others demonstrated that the Fur transcription factor is required for activation of SPI-1 genes (35–38). Therefore, we determined the effect of Fur on the expression of the PhilC-lacZ, PrtsA-lacZ, and PhilD-lacZ fusions following growth at 37°C. Because growth at 42°C repressed expression of the PrtsA-lacZ fusion, identifying that Fur also regulates SPI-1 in this manner would suggest that temperature control of SPI-1 may act through Fur. However, activation of the PrtsA-lacZ and PhilD-lacZ fusions was inhibited by deletion of the fur gene (Fig. 4A). The reduction in PrtsA and PhilD activation was consistent with earlier data, which showed that Fur regulated SPI-1 by controlling hilD expression when the hilD gene was present (35, 37). Following growth at 37°C and consistent with earlier findings (35, 36), the overexpression of Fur increased expression of hilA-lacZ by ∼4-fold (Fig. 4B, right panel). Despite the enhanced expression of the hilA-lacZ fusion following induction of the Fur protein with IPTG at 37°C, induction at 42°C did not increase expression of hilA-lacZ even though the levels of the Fur protein under the two sets of conditions were strikingly similar (Fig. 4B, right panel). These data indicated that the inability to activate SPI-1 following growth at 42°C was not related to Fur.

Growth at 42°C repressed expression of SPI-1 genes independently of the activator Fur. (A) The promoters of hilC, rtsA, and hilD were cloned into the pSP417 multicopy shuttle vector (empty vector) upstream of a promoterless lacZ gene. Bacteria were grown as described for Fig. 1B, and the promoter activities were determined for the NC1040 and fur::cat strains following overnight growth at 37°C. Data are from 3 separate experiments. The strains used were BTNC0002 to BTNC0005 and BTNC0006 to BTNC0009. (B) Expression of a hilA-lacZ fusion at the chromosomal att site was determined following overnight growth with or without induction of the Fur-FLAG protein. Bacteria were grown as described for Fig. 1B, except that samples were diluted 500-fold and cultivated at either 37°C or 42°C. A portion of each sample was removed to measure β-galactosidase activity, and the remainder was treated for SDS-PAGE and Western blotting to detect the FLAG epitope. Following transfer of proteins to the nitrocellulose membrane, the membrane was stained with Ponceau S to ensure that equivalent levels of protein were loaded for samples and that ∼2 × 108 cells were loaded per lane (left panel). IPTG was added to the growth medium to reach a concentration of 0.1 mM to induce Fur-FLAG. Western blotting with the anti-FLAG antibody revealed cross-reactivity to the Fur protein of the expected size, indicated by the arrowhead with the appropriate label (right panel). The β-galactosidase activity for each sample is listed below each lane (right panel). Samples shown are representative of the results of 3 separate experiments. The complete β-galactosidase activity data are listed here. For BTNC0017 (pfur-flag), the values measured at 37°C were 156 ± 33 under uninduced conditions and 657 ± 89 under induced conditions and the values measured at 42°C were 316 ± 70 under uninduced conditions and 345 ± 4 under induced conditions.

How To Use an Infrared Thermometer Olympia laser testing Surface Body Temperature of Chicks Chickens

FAQ

What is the normal body temperature of a chicken?

Understanding the normal body temperature of a chicken is vital for their optimal health and well-being. With an average body temperature ranging from 104 to 107 degrees Fahrenheit, chickens possess unique physiological adaptations to thrive in diverse environments.

What temperature does a feathered chicken eat?

The core, or deep body, temperature of a fully feathered chicken normally ranges between 105 and 107 degrees, averaging 106 degrees under normal circumstances. Sometimes the upper limit is as high as 109 or even 113 degrees. The reason has to do with the increased growth rate of modern Cornish Cross broilers compared with a decade ago.

How hot does a chicken run?

Chickens are naturally warm-blooded, with an average body temperature between 105-107°F (40-42°C). Yep, they run hotter than your morning coffee. This internal furnace helps them thrive even when the temperatures outside feel more fit for a polar bear than a poultry party.

Do chickens have a higher body temperature than humans?

As mentioned earlier, chickens have higher body temperature than human beings—a healthy chicken temperature averages at 106 degrees Fahrenheit, compared to a human’s 100. However, the temperature varies a little, depending on stress leaven, the recency of the last meal, and the time of the day, as it does in people.

Do baby chicks have a similar body temperature?

Yes, baby chicks have a similar body temperature to adult chickens. The average body temperature range of 104 to 107 degrees Fahrenheit applies to both chicks and adults. 11. Can fluctuating temperatures in their environment affect a chicken’s health? Extreme temperature fluctuations can be detrimental to a chicken’s health.

What if my chicken’s body temperature drops below a normal range?

If you notice a significant drop in your chicken’s body temperature below the normal range, it could be an indication of illness or stress. For instance, if your chicken’s temperature drops to 100°F (38°C) or lower, it may be experiencing symptoms such as lethargy, loss of appetite, or labored breathing.

What animal has the highest body temperature?

How do chickens regulate body temperature?

What is the 90/10 rule for chickens?

The 90/10 rule for chickens states that 90% of a chicken’s diet should come from a balanced, complete poultry feed, while the remaining 10% can be made up of treats, such as garden scraps, fruits, vegetables, or scratch grains. This rule ensures that chickens receive all the essential nutrients they need for growth, health, and egg production without diluting their diet with too many nutritionally empty extras.

What is the body temperature of a hen?