Probiotic Bacillus subtilis on Laying Hens: Comparison
Please note this is a comparison between Version 2 by Amina Yu and Version 1 by Sha Jiang.

Bacillus subtilisis one of the three most common species of probiotic products in the U.S. and has been used widely as a functional feed supplement such as in several dairy and non-dairy fermented foods for improving human health and well-being. Similarly, Bacillus subtilis-based probiotics have been used as antibiotic growth promoter alternatives in poultry. Bacillus subtilis are spore-forming bacteria. They are heat stable, low pH-resistant (the gastric barrier), and tolerate multiple environmental stressors.

  • chicken
  • social stress
  • serotonin
  • probiotic

1. Production Environments and Related Stress in Commercial Laying Hens 

Chickens as well as other farm animals are constantly selected by both nature (natural selection) and humans (artificial selection). During selection, the animals’ biological and behavioral characteristics have been constantly changed [1,2][1][2]. The process is affected by multiple factors including their surrounding environments, by which the animals have been selected for increased fitness (that is survival and reproductive success) over generations.

Commercial chickens have been selected for production (laying hens for eggs and broilers for meat) to meet the increasing demand for poultry products [3,4][3][4]. The consumption of chicken meat and eggs represents cheap, healthy, and quality protein sources in human nutrition globally. However, the breeding programs may subject chickens to physiological dysfunction and immunosuppression by simply focusing on reproduction and or growth rates [5[5][6],6], subsequently increasing susceptibility to metabolic disorders and management-associated stressors [7,8][7][8]. For example, a laying hen produces approximately 310 eggs annually with a low feed consumption of just 110 g per day [9]. The extreme selection for one trait (production) could affect other biological traits, causing negative impacts on animal health and welfare such as aggression and related injurious behavior [10]. Selection for production increases aggression as, from an evolutionary point of view, aggression in animals is a natural behavior associated with competition to deal with life-threating situations affecting an individual’s survival, growth, and reproductive success within a group [11,12][11][12]. Controversially, selection based on hen behavior may reduce feather pecking, but it may result in an unfavorable correlated selection response, reducing egg production [13].

Currently, the conventional (battery) cage system is the most common housing facility for laying hens in the United Sates (U.S.), which was estimated to be 70.7% of the table egg layer flocks (approximately 231.7 million laying hens) at the end of 2020 [14]. Typically, commercial laying hens are housed in groups ranging from five to nine birds per cage or greater at a density of 67–86 in2/hen, starting at about 18 weeks of age. The high stocking density of hens and limited space for hens to display their “natural” behavior (such as foraging, exploration, perching, and nesting) negatively impact their welfare status, resulting in a chronic state of stress [15]. One of the possible strategies to improve hen health and welfare is to modify their rearing environments, and several alternatives to the conventional cage system have been developed such as enriched cage system (consisting of a nest, litter bath or scratch area, perches, and abrasive strip) and cage-free systems with or without outdoor access such as aviaries (single- and multiple-tiered) [16]. Although hens housed in the enriched cage system and non-cage systems seem to be possible ways to improve their welfare by displaying some degree of “natural” behavior such as nesting, roosting, and scratching [17[17][18],18], there is a high risk of increased exhibition of injurious behavior (feather pecking, aggression, and cannibalism) resulting from large group sizes and social instability [19,20,21,22,23][19][20][21][22][23]. Social stress and associated injurious behavior are major concerns in all current housing environments including cage and cage-free systems [19,20][19][20].

2. Probiotics, Bacillus subtilis-Based Probiotics, Social Challenge-Induced Aggression

2. Probiotics, Bacillus subtilis-Based Probiotics, Social Challenge-Induced Aggression

Probiotics are commensal bacteria (“direct-fed microbials”, DFM) that offer potential health beneficial effects to the host’s stress response (acute, chronic or both). Several commercial probiotics have been used in poultry production [24[24][25],25], and numerous studies have shown that probiotics aid chickens in adapting to their environment and improving their health and welfare by: (1) altering the microbiota profile with beneficial bacteria to prevent the growth of pathogens and to compete with enteric pathogens for the limited availability of nutrient and attachment sites; (2) producing bacteriocins (such as bacteriostatic and bactericidal substances) with antimicrobial function and short chain fatty acids to regulate the activity of intestinal digestive enzymes and energy homeostasis; (3) modulating gut and systemic immunity; (4) restoring the intestinal barrier integrity preventing pathogens from crossing the mucosal epithelium; (5) stimulating the endocrine system and attenuating stress-induced disorders of the HPA and/or sympathetic-adrenal-medullary (SMA) axes via the gut–brain axis; (6) inducing epithelial heat shock proteins to protect cells from oxidative damage; and (7) synthesis and secretion of neurotransmitters such as 5-HT and tryptophan [26,27,28,29,30][26][27][28][29][30].

It has been stated in humans and non-human primates that the gut microbiota have potential effects on their hosts’ aggressive behaviors and anxiety symptoms [31,32,33][31][32][33]. In rodent studiones, germ-free (GF) animals with exaggerated HPA responses to social stress can be normalized by certain probiotics [34,35,36][34][35][36]. In addition, probiotics have successfully attenuated anxiety and depressive behaviors in rat offspring separated from their mother [37,38][37][38] and the obsessive-compulsive-like behaviors in mice [39,40][39][40]. These results support the psychobiotics theory [41,42][41][42] (i.for example., a special class of probiotics (beneficial bacteria) delivering mental and cognitive health benefits (such as anxiolytic and antidepressant effects) to individuals) and provide a potential to use probiotics as a biotherapeutic strategy for improving a host’s mental and cognitive function in humans and other animals including chickens [43,44,45,46,47,48,49,50][43][44][45][46][47][48][49][50]. Probiotics may have similar effects on chicken behavior due to the human–animal transmission occurs during the evolution and ecology of gastrointestinal microbial development (the host–microbial coevolution) [51,52][51][52]. Several probiotics have been used in preventing injurious damage in poultry. For example, probiotic Lactobacillus rhamnosus JB-1 supplementation (5 × 109/mL in drinking water provided from week 19 to week 28) reduces chronic stress (social disruption, physical and manual restraint, and blocking nest boxes and perch usage applied from week 24 to week 26) induced feather pecking and cecal microbiota dysbiosis, along with increased T cell populations in the spleen and cecal tonsils of adult chickens regardless of the genetic lines (HFP and LFP lines) [53]. Probiotic LactobacilluLactobacillus rhamnosus s rhamnosus supplement (applied from day 1 to week 9) also counteracted stress-induced decrease in T cells, along with a short-term (from week 10 to week 13) increase in plasma tryptophan and the TRP:(PHE + TYR) ratio (from week 14 to week 15), but without effects on feather pecking in pullets [34]. The TRP:(PHE  +  TYR) ratio has been used as an indicator of the competition between tryptophan and other amino acids for uptake across the BBB [54]. In addition, the number of feather pecking bouts was positively correlated with intestinal contraction velocity and amplitude in peckers, which can be modulated by administrated L. L. rhamnosus rhamnosus [55][55]Lactobacillus-based probiotic supplements also reduced stress-associated immobility behavior in rodents during the forced swine test [56]. Parois et al. [57] [57] also reported that probiotic PediococcusPediococcus acidilactici acidilactici reduced fearfulness in selected short tonic immobility birds, indicated by a short immobility during the tonic immobility test via regulation of the MGB axis. Reduced fearfulness was also found in a synbiotic studyone [58]. It consisted of a probiotic (EnterococcusEnterococcus faecium, Pediococcus acidilactici, Bifidobacterium animalis, faecium, Pediococcus acidilactici, Bifidobacterium animalis, and Lactobacillus reuteri) and a prebiotic (fructooligosaccharides). The synbiotic fed broilers had a shorter latency to make the first vocalization with a higher vocalization rate during an isolation test, and a greater number of synbiotic fed birds reached the observer during a touch test. There results revealed a potential strategy to use probiotics to reduce stress response and stress-induced injurious behavior during poultry production. However, large gaps about probiotic functions in improving neuropsychiatric disorders remain, which are affected by multiple factors including the type of probiotic bacteria and duration and dosage of the intervention.

Bacillus2.1. subtilisBacillus subtilis

Bacillus subtilis is one of the three most common species of probiotic products in the U.S. [59] and has been used widely as a functional feed supplement such as in several dairy and non-dairy fermented foods for improving human health and well-being [60,61,62,63][60][61][62][63]. Similarly, Bacillus subtilis Bacillus subtilis-based probiotics have been used as antibiotic growth promoter alternatives in poultry [64,65,66,67][64][65][66][67]. Bacillus Bacillus subtilis subtilis are spore-forming bacteria. They are heat stable, low pH-resistant (the gastric barrier), and tolerate multiple environmental stressors [68,69][68][69]. Several mechanisms of actions of Bacillus s Bacillus sppp. have been proposed: regulating intestinal microstructure [70] [70] and digestive enzymes [71,72][71][72]; synthesizing and releasing antimicrobial and antibiotic compounds [65]; increasing immunity [71[71][73][74],73,74], and neurochemical activities including 5-HT [75,76,77][75][76][77] as well as affecting animal behavior [76] [76]following various stressors. For example, in response stimulations, Bacillus Bacillus subtilis subtilis alleviates oxidative stress, provokes a specific biological response, and improves the mood status of hosts via the gut–brain axis [78,79][78][79]. In addition, Bacillus Bacillus subtilis subtilis can overproduce L-tryptophan [80[80][81][82],81,82], and consequently increase 5-HT in the hypothalamus [83]. Tryptophan functions as an antidepressant and anti-anxiety agent [83,84,85,86] [83][84][85][86] and eliminates nervous tension in mice [87,88][87][88]. In one study, chickens were used as an animal model to assess whether dietary supplementation of the probiotic Bacillus subtilis  Bacillus subtilis reduced aggressive behaviors following social challenge [89].

Chickens, as social animals, show fear, depression, and or anxiety in novel environments [52] [52]and show aggression toward others for establishing aa social dominance rank in unfamiliar social groups [90[90][91][92],91,92], which is similar to the rodents used in human psychopharmacological studiones [93,94,95][93][94][95]. The paired social ranking-associated behavioral test used in this studyone [85] has been routinely performed in chicken behavioral analysis [80,96,97][80][96][97]. The rationale of the test is similar to the resident-intruder test, which is a standardized method used in rodents for detecting social stress-induced aggression and violence [98,99,100,101][98][99][100][101].

In the istudy [87], the role of the probiotic Bacillus subtilis on the aggression in hens of the Dekalb XL (DXL) line was examined. One-day-old female chicks were kept in single-bird cages [89]. The hens at 24-weeks-old were paired based on their body weight for the first behavioral test (pre-probiotic treatment, day 0) in a novel floor pen. To determine the dominant individual per pair, behaviors were video-taped for 2 h immediately after the release of two hens simultaneously into the floor pen. After the test, the subordinate and dominant hens were fed the regular diet or the diet mixed with 250 ppm probiotic (1.0 × 106 cfu/g of feed) for two weeks, respectively. The probiotic contained three proprietary strains of Bacillus subtilis (Sporulin®, Novus International Inc., Saint Charles, MO, USA). After the treatment (day 14), the second aggression test was conducted within the same pair of hens. The injurious behaviors were detected and analyzed.

TheIt resultswas indicated that compared to their initial levels at day 0, the levels of threat kick were reduced, the frequency of aggressive pecking tended to be lower, and the levels of feather pecking was reduced but without statistical significance in probiotic fed dominant hens. There was no change in injurious behaviors in the regular diet fed subordinate hens between day 0 and day 14. The behavioral changes in probiotic fed dominant hens were correlated with the changes in blood 5-HT concentrations. Post-treatment (day 14), plasma 5-HT levels were reduced toward the levels of the controls (subordinates) in the probiotic fed dominant hens compared to their related levels prior to treatment (day 0). Similarly, the effects of probiotic dietary supplements on behavior have been found in turkeys [98]. The turkey poults fed probiotic Bacillus amyloliquefaciens had increased feeding frequency and duration with decreased distress call and aggressive behavior.

The similar relations between reduced aggressive behavioral exhibition and blood 5-HT concentrations were identified in ourthe previous studiones [10[10][102],102], genetic selection for prevention of social stress-induced feather pecking, and aggression. Compared to MBB mean bad birds (MBB), kind gentle birds (KGB) had lower blood 5-HT concentrations as well as lower concentrations of blood dopamine (DA) and corticosterone (CORT) and a lower heterophil/lymphocyte (H/L) ratio, a stress marker, with lower frequency of injurious pecking [10,103][10][103]. Bolhuis et al. [104] [104] also reported that peripheral serotonin activity reflected the predisposition to develop severe feather pecking in laying hens. Similarly, individuals with a lower blood 5-HT level that showed less aggressiveness were found in humans [105,106,107][105][106][107] and canine [108] [108] while an elevated level of blood 5-HT has been revealed in patients with aggressive behavior [109,110][109][110] and in aggressive teleost fish [111]. These results provide evidence for serotonergic mediation for aggressive behavior and stress coping strategy; and chicken aggression can be reduced or inhibited by probiotic supplementation by directly or indirectly regulating the serotonergic system.

Whether the changes in blood 5-HT levels in probiotic fed dominant hens represent a similar change in 5-HT concentrations in the brain is unclear as 5-HT cannot pass the blood–brain barrier and is regulated differently between brain neurons and peripheral tissues [112]. The plasma 5-HT is synthesized mainly by the enterochromaffin (EC) cells (also known as Kulchitsky cells), types of enteroendocrine and neuroendocrine cells, of the gut and stored in the platelets [113]. However, it has been proposed that platelet 5-HT uptake is a limited peripheral marker of brain serotonergic synaptosomes [112]Lactobacillus plantarum strain PS128, a dietary probiotic that causes an increase in the levels of striatal 5-HT as well as DA, is correlated with improving anxiety-like behavior in germ-free (GF) mice [113]. Similar results have been obtained from our current studies [89,114][89][114]. In another studyone, chickens (broilers) were fed Bacillus Bacillus subtilis subtilis from day 1 to day 43. The results indicate that Bacillus Bacillus subtilis subtilis fed chickens had higher levels of 5-HT in the raphe nuclei and lower levels of norepinephrine (NE) and DA in the hypothalamus compared to the controls fed a regular diet [113]. Probiotic fed chickens also had improved skeletal traits (bone mineral density, bone mineral content and robusticity index). In one heat stress (32 °C for 10 h) study, Bacillus subtilisBacillus subtilis fed chickens (broilers) had lower heat stress-related behaviors including panting and wing spreading and inflammatory response in the hypothalamus compared to the controls [82]. Further studies, however, are needed to examine how the correlations present between injurious behavior and peripheral and or brain 5-HT in probiotic fed chickens.

 

References

  1. Kaiser, S.; Hennessy, M.B.; Sachser, N. Domestication affects the structure, development and stability of biobehavioural profiles. Front. Zool. 2015, 12, S19.
  1. Travis, J.; Reznick, D.N. Natural Selection: How Selection on behaviour interacts with selection on morphology. Curr. Biol. 2018, 28, R882–R884.
  2. Davis, T.C.; White, R.R.; Breeding animals to feed people: The many roles of animal reproduction in ensuring global food security. Theriogenology 2020, 150, 27–33.
  3. Ramachandran, R. Current and future reproductive technologies for avian species. Adv. Exp. Med. Biol. 2014, 752, 23–31.
  4. Webster, A.B. Welfare implications of avian osteoporosis. Poult. Sci. 2004, 83, 184–192.
  5. Bain, M.M.; Nys, Y.; Dunn, I.C. Increasing persistency in lay and stabilising egg quality in longer laying cycles. What are the challenges? Br. Poult. Sci. 2016, 57, 330–338.
  6. Moreira, G.C.M.; Salvian, M.; Boschiero, C.; Cesar, A.S.M.; Reecy, J.M.; Godoy, T.F.; Ledur, M.C.; Garrick, D.; Mourão, G.B.; Coutinho, L.L. Genome-wide association scan for QTL and their positional candidate genes associated with internal organ traits in chickens. BMC Genom. 2019, 20, 669.
  7. Rubio, L.A. Possibilities of early life programming in broiler chickens via intestinal microbiota modulation. Poult. Sci. 2019, 98, 695–706.
  8. UEP (United Egg Producers). Animal Husbandry Guidelines for U.S. Egg-Laying Hens. 2017 Edition. Available online: https://uepcertified.com/wp-content/uploads/2019/09/CF-UEP-Guidelines_17-3.pdf (accessed on 20 December 2021).
  9. Cheng, H.W.; Muir, W.M. Mechanisms of aggression and production in chickens: Genetic variations in the functions of serotonin, catecholamine, and corticosterone. World’s Poult. Sci. J. 2007, 63, 233–254.
  10. Veroude, K.; Zhang-James, Y.; Fernàndez-Castillo, N.; Bakker, M.J.; Cormand, B.; Faraone, S.V. Genetics of aggressive behaviour: An overview. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2016, 171, 3–43.
  11. Foister, S.; Doeschl-Wilson, A.; Roehe, R.; Arnott, G.; Boyle, L.; Turner, S. Social network properties predict chronic aggression in commercial pig systems. PLoS ONE 2018, 13, e0205122.
  12. Bennewitz, J.; Bögelein, S.; Stratz, P.; Rodehutscord, M.; Piepho, H.P.; Kjaer, J.B.; Bessei, W. Genetic parameters for feather pecking and aggressive behaviour in a large F2-cross of laying hens using generalized linear mixed models. Poult. Sci. 2014, 93, 810–817.
  13. UEP (Unite Egg Producers). Facts and Stats. 2020. Available online: https://unitedegg.com/facts-stats/ (accessed on 12 January 2022).
  14. Blatchford, R.A.; Fulton, R.M.; Mench, J.A. The utilization of the Welfare Quality® assessment for determining laying hen condition across three housing systems. Poult. Sci. 2016, 95, 154–163.
  15. Widmar, N.; Bir, C.; Wolf, C.; Lai, J.; Liu, Y. #Eggs: Social and online media-derived perceptions of egg-laying hen housing. Poult. Sci. 2020, 99, 5697–5706.
  16. Appleby, M.C.; Walker, A.W.; Nicol, C.J.; Lindberg, A.C.; Freire, R.; Hughes, B.O.; Elson, H.A. Development of furnished cages for laying hens. Br. Poult. Sci. 2002, 43, 489–500.
  17. Campbell, D.L.M.; Hinch, G.N.; Downing, J.A.; Lee, C. Early enrichment in free-range laying hens: Effects on ranging behaviour, welfare and response to stressors. Animal 2018, 12, 575–584.
  18. Coton, J.; Guinebretière, M.; Guesdon, V.; Chiron, G.; Mindus, C.; Laravoire, A.; Pauthier, G.; Balaine, L.; Descamps, M.; Bignon, L.; et al. Feather pecking in laying hens housed in free-range or furnished-cage systems on French farms. Br. Poult. Sci. 2019, 60, 617–627.
  19. Schreiter, R.; Damme, K.; von Borell, E.; Vogt, I.; Klunker, M.; Freick, M. Effects of litter and additional enrichment elements on the occurrence of feather pecking in pullets and laying hens—A focused review. Vet. Med. Sci. 2019, 5, 500–507.
  20. van Staaveren, N.; Ellis, J.; Baes, C.F.; Harlander-Matauschek, A. A meta-analysis on the effect of environmental enrichment on feather pecking and feather damage in laying hens. Poult. Sci. 2021, 100, 397–411.
  21. Brantsæter, M.; Nordgreen, J.; Hansen, T.B.; Muri, K.; Nødtvedt, A.; Moe, R.O.; Janczak, A.M. Problem behaviours in adult laying hens—Identifying risk factors during rearing and egg production. Poult. Sci. 2018, 97, 2–16.
  22. Zepp, M.; Louton, H.; Erhard, M.; Schmidt, P.; Helmer, F.; Schwarzer, A. The influence of stocking density and enrichment on the occurrence of feather pecking and aggressive pecking behaviour in laying hen chicks. J. Vet. Behav. 2018, 24, 9–18.
  23. Jha, R.; Das, R.; Oak, S.; Mishra, P. Probiotics (direct-fed microbials) in poultry nutrition and their effects on nutrient utilization, growth and laying performance, and gut health: A systematic review. Animals 2020, 10, 1863.
  24. Krysiak, K.; Konkol, D.; Korczyński, M. Overview of the Use of Probiotics in Poultry Production. Animals 2021, 11, 1620.
  25. Bindari, Y.R.; Gerber, P.F. Centennial Review: Factors affecting the chicken gastrointestinal microbial composition and their association with gut health and productive performance. Poult. Sci. 2022, 101, 101612.
  26. Shehata, A.A.; Yalçın, S.; Latorre, J.D.; Basiouni, S.; Attia, Y.A.; Abd El-Wahab, A.; Visscher, C.; El-Seedi, H.R.; Huber, C.; Hafez, H.M.; et al. Probiotics, Prebiotics, and Phytogenic Substances for Optimizing Gut Health in Poultry. Microorganisms 2022, 10, 395.
  27. Villageliu, D.N.; Lyte, M. Microbial endocrinology: Why the intersection of microbiology and neurobiology matters to poultry health. Poult. Sci. 2017, 96, 2501–2508.
  28. Lyte, J.M.; Martinez, D.A.; Robinson, K.; Donoghue, A.M.; Daniels, K.M.; Lyte, M. A neurochemical biogeography of the broiler chicken intestinal tract. Poult. Sci. 2022, 101, 101671.
  29. Khan, S.; Moore, R.J.; Stanley, D.; Chousalkar, K.K. The Gut Microbiota of Laying Hens and Its Manipulation with Prebiotics and Probiotics To Enhance Gut Health and Food Safety. Appl. Environ. Microbiol. 2020, 86, e00600-20.
  30. Sylvia, K.E.; Demas, G.E. A gut feeling: Microbiome-brain-immune interactions modulate social and affective behaviours. Horm. Behav. 2018, 99, 41–49.
  31. Ren, C.C.; Sylvia, K.E.; Munley, K.M.; Deyoe, J.E.; Henderson, S.G.; Vu, M.P.; Demas, G.E. Photoperiod modulates the gut microbiome and aggressive behaviour in Siberian hamsters. J. Exp. Biol. 2020, 223, jeb212548.
  32. Pirbaglou, M.; Katz, J.; de Souza, R.J.; Stearns, J.C.; Motamed, M.; Ritvo, P. Probiotic supplementation can positively affect anxiety and depressive symptoms: A systematic review of randomized controlled trials. Nutr. Res. 2016, 36, 889–898.
  33. Mindus, C.; van Staaveren, N.; Fuchs, D.; Gostner, J.M.; Kjaer, J.B.; Kunze, W.; Mian, M.F.; Shoveller, A.K.; Forsythe, P.; Harlander-Matauschek, A.L. rhamnosus improves the immune response and tryptophan catabolism in laying hen pullets. Sci. Rep. 2021, 11, 19538.
  34. Cryan, J.F.; Dinan, T.G. Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 2012, 13, 701–712.
  35. Rincel, M.; Darnaudery, M. Maternal separation in rodents: A journey from gut to brain and nutritional perspectives. Proc. Nutr. Soc. 2020, 79, 113–132.
  36. Slykerman, R.F.; Hood, F.; Wickens, K.; Thompson, J.M.D.; Barthow, C.; Murphy, R.; Kang, J.; Rowden, J.; Stone, P.; Crane, J.; et al. Effect of Lactobacillus rhamnosus HN001 in pregnancy on postpartum symptoms of depression and anxiety: A randomised double-blind placebo-controlled trial. EBioMedicine 2017, 24, 159–165.
  37. Sanders, A.; Rackers, H.; Kimmel, M. A role for the microbiome in mother-infant interaction and perinatal depression. Int. Rev. Psychiatry 2019, 31, 280–294.
  38. Kantak, P.A.; Bobrow, D.N.; Nyby, J.G. Obsessive-compulsive-like behaviours in house mice are attenuated by a probiotic (Lactobacillus rhamnosus GG). Behav. Pharmacol. 2014, 25, 71–79.
  39. Latalova, K.; Hajda, M.; Prasko, J. Can gut microbes play a role in mental disorders and their treatment? Psychiatria Danub. 2017, 29, 28–30.
  40. Tremblay, A.; Lingrand, L.; Maillard, M.; Feuz, B.; Tompkins, T.A. The effects of psychobiotics on the microbiota-gut-brain axis in early-life stress and neuropsychiatric disorders. Prog. Neuropsychopharmacol. Biol. Psychiatry 2021, 105, 110142.
  41. Nikolova, V.L.; Hall, M.R.B.; Hall, L.J.; Cleare, A.J.; Stone, J.M.; Young, A.H. Perturbations in gut microbiota composition in psychiatric disorders: A review and meta-analysis. JAMA Psychiatry 2021, 78, 1343–1354.
  42. Tian, P.; O’Riordan, K.J.; Lee, Y.K.; Wang, G.; Zhao, J.; Zhang, H.; Cryan, J.F.; Chen, W. Towards a psychobiotic therapy for depression: Bifidobacterium breve CCFM1025 reverses chronic stress-induced depressive symptoms and gut microbial abnormalities in mice. Neurobiol. Stress 2020, 12, 100216.
  43. Yadav, M.; Mandeep; Shukla, P. Probiotics of diverse origin and their therapeutic applications: A review. J. Am. Coll. Nutr. 2020, 39, 469–479.
  44. Zagórska, A.; Marcinkowska, M.; Jamrozik, M.; Wiśniowska, B.; Paśko, P. From probiotics to psychobiotics—The gut-brain axis in psychiatric disorders. Benef. Microbes 2020, 11, 717–732.
  45. Ligezka, A.N.; Sonmez, A.I.; Corral-Frias, M.P.; Golebiowski, R.; Lynch, B.; Croarkin, P.E.; Romanowicz, M. A systematic review of microbiome changes and impact of probiotic supplementation in children and adolescents with neuropsychiatric disorders. Prog. Neuropsychopharmacol. Biol. Psychiatry 2021, 108, 110187.
  46. Ruiz-Gonzalez, C.; Roman, P.; Rueda-Ruzafa, L.; Rodriguez-Arrastia, M.; Cardona, D. Effects of probiotics supplementation on dementia and cognitive impairment: A systematic review and meta-analysis of preclinical and clinical studies. Prog. Neuropsychopharmacol. Biol. Psychiatry 2021, 108, 110189.
  47. Sharma, R.; Gupta, D.; Mehrotra, R.; Mago, P. Psychobiotics: The next-generation probiotics for the brain. Curr. Microbiol. 2021, 78, 449–463.
  48. Berding, K.; Cryan, J.F. Microbiota-targeted interventions for mental health. Curr. Opin. Psychiatry 2022, 35, 3–9.
  49. Deidda, G.; Biazzo, M. Gut and Brain: Investigating physiological and pathological interactions between microbiota and brain to gain new therapeutic avenues for brain diseases. Front. Neurosci. 2021, 15, 753915.
  50. Ellis, R.J.; Bruce, K.D.; Jenkins, C.; Stothard, J.R.; Ajarova, L.; Mugisha, L.; Viney, M.E. Comparison of the distal gut microbiota from people and animals in Africa. PLoS ONE 2013, 8, e54783.
  51. Reese, A.T.; Chadaideh, K.S.; Diggins, C.E.; Schell, L.D.; Beckel, M.; Callahan, P.; Ryan, R.; Emery Thompson, M.; Carmody, R.N. Effects of domestication on the gut microbiota parallel those of human industrialization. Elife 2021, 10, e60197.
  52. Mindus, C.; van Staaveren, N.; Bharwani, A.; Fuchs, D.; Gostner, J.M.; Kjaer, J.B.; Kunze, W.; Mian, M.F.; Shoveller, A.K.; Forsythe, P.; et al. Ingestion of Lactobacillus rhamnosus modulates chronic stress-induced feather pecking in chickens. Sci. Rep. 2021, 11, 17119.
  53. Wurtman, R.J.; Hefti, F.; Melamed, E. Precursor control of neurotransmitter synthesis. Pharmacol. Rev. 1980, 32, 315–335.
  54. van Staaveren, N.; Krumma, J.; Forsythe, P.; Kjaer, J.B.; Kwon, I.Y.; Mao, Y.K.; West, C.; Kunze, W.; Harlander-Matauschek, A. Cecal motility and the impact of Lactobacillus in feather pecking laying hens. Sci. Rep. 2020, 10, 12978.
  55. Mindus, C.; Ellis, J.; van Staaveren, N.; Harlander-Matauschek, A. Lactobacillus-Based Probiotics Reduce the Adverse Effects of Stress in Rodents: A Meta-analysis. Front. Behav. Neurosci. 2021, 15, 642757.
  56. Parois, S.; Calandreau, L.; Kraimi, N.; Gabriel, I.; Leterrier, C. The influence of a probiotic supplementation on memory in quail suggests a role of gut microbiota on cognitive abilities in birds. Behav. Brain Res. 2017, 331, 47–53.
  57. Mohammed, A.; Mahmoud, M.; Murugesan, R.; Cheng, H.W. Effect of a Synbiotic Supplement on Fear Response and Memory Assessment of Broiler Chickens Subjected to Heat Stress. Animals 2021, 11, 427.
  58. Joerger, R.D.; Ganguly, A. Current status of the preharvest application of pro- and prebiotics to farm animals to enhance the microbial safety of animal products. Microbiol. Spectr. 2017, 5. https://doi.org/10.1128/microbiolspec.PFS-0012-2016.
  59. Jeżewska-Frąckowiak, J.; Seroczyńska, K.; Banaszczyk, J.; Jedrzejczak, G.; Żylicz-Stachula, A.; Skowron, P.M. The promises and risks of probiotic Bacillus species. Acta Biochim. Pol. 2018, 65, 509–519.
  60. Campbell, D.L.M.; Dickson, E.J.; Lee, C. Application of open field, tonic immobility, and attention bias tests to hens with different ranging patterns. PeerJ 2019, 7, e8122.
  61. Paytuví-Gallart, A.; Sanseverino, W.; Winger, A.M. Daily intake of probiotic strain Bacillus subtilis DE111 supports a healthy microbiome in children attending day-care. Benef. Microbes 2020, 11, 611–620.
  62. Trotter, R.E.; Vazquez, A.R.; Grubb, D.S.; Freedman, K.E.; Grabos, L.E.; Jones, S.; Gentile, C.L.; Melby, C.L.; Johnson, S.A.; Weir, T.L. Bacillus subtilis DE111 intake may improve blood lipids and endothelial function in healthy adults. Benef. Microbes 2020, 11, 621–630.
  63. Abd El-Hack, M.E.; El-Saadony, M.T.; Shafi, M.E.; Qattan, S.Y.A.; Batiha, G.E.; Khafaga, A.F.; Abdel-Moneim, A.E.; Alagawany, M. Probiotics in poultry feed: A comprehensive review. J. Anim. Physiol. Anim. Nutr. 2020, 104, 1835–1850.
  64. Park, I.; Lee, Y.; Goo, D.; Zimmerman, N.P.; Smith, A.H.; Rehberger, T.; Lillehoj, H.S. The effects of dietary Bacillus subtilis supplementation, as an alternative to antibiotics, on growth performance, intestinal immunity, and epithelial barrier integrity in broiler chickens infected with Eimeria maxima. Poult. Sci. 2020, 99, 725–733.
  65. Jiang, S.; Yan, F.F.; Hu, J.Y.; Mohammed, A.; Cheng, H.W. Bacillus subtilis-based probiotic improves skeletal health and immunity in broiler chickens exposed to heat stress. Animals 2021, 11, 1494.
  66. Neveling, D.P.; Dicks, L.M.T. Probiotics: An antibiotic replacement strategy for healthy broilers and productive rearing. Probiotics Antimicrob. Proteins 2021, 13, 1–11.
  67. Cartman, S.T.; La Ragione, R.M.; Woodward, M.J. Bacillus subtilis spores germinate in the chicken gastrointestinal tract. Appl. Environ. Microbiol. 2008, 74, 5254–5258.
  68. Mingmongkolchai, S.; Panbangred, W. Bacillus probiotics: An alternative to antibiotics for livestock production. J. Appl. Microbiol. 2018, 124, 1334–1346.
  69. Samanya, M.; Yamauchi, K. Histological alterations of intestinal villi in chickens fed dried Bacillus subtilis var. natto. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2002, 133, 95–104.
  70. Fernandez-Alarcon, M.F.; Trottier, N.; Steibel, J.P.; Lunedo, R.; Campos, D.M.B.; Santana, A.M.; Pizauro, J.M., Jr.; Furlan, R.L.; Furlan, L.R. Interference of age and supplementation of direct-fed microbial and essential oil in the activity of digestive enzymes and expression of genes related to transport and digestion of carbohydrates and proteins in the small intestine of broilers. Poult. Sci. 2017, 96, 2920–2930.
  71. Bar Shira, E.; Friedman, A. Innate immune functions of avian intestinal epithelial cells: Response to bacterial stimuli and localization of responding cells in the developing avian digestive tract. PLoS ONE 2018, 13, e0200393.
  72. Abudabos, A.M.; Aljumaah, M.R.; Alkhulaifi, M.M.; Alabdullatif, A.; Suliman, G.M.; Al Sulaiman, A.R. Comparative effects of Bacillus subtilis and Bacillus licheniformis on live performance, blood metabolites and intestinal features in broiler inoculated with Salmonella infection during the finisher phase. Microb. Pathog. 2019, 139, 103870.
  73. Galagarza, O.A.; Smith, S.A.; Drahos, D.J.; Eifert, J.D.; Williams, R.C.; Kuhn, D.D. Modulation of innate immunity in Nile tilapia (Oreochromis niloticus) by dietary supplementation of Bacillus subtilis endospores. Fish Shellfish Immunol. 2018, 83, 171–179.
  74. Lyte, M. Probiotics function mechanistically as delivery vehicles for neuroactive compounds: Microbial endocrinology in the design and use of probiotics. Bioessays 2011, 33, 574–581.
  75. Fan, W.-J.; Li, Y.-T.; Chen, J.-J.J.; Chen, S.-C.; Lin, Y.S.; Kou, Y.R.; Peng, C.-W. Sexually dimorphic urethral activity in response to pharmacological activation of 5-HT1A receptors in the rat. Am. J. Physiol. Renal Physiol. 2013, 305, F1332–F1342.
  76. Gong, Q.; Liu, L.; Janowski, M. Dopaminergic and serotoninergic signaling in black fur BL6 and albino, rag2-/-, immunodeficient BL6 mice subjected to lens-induced (LIM) and form-deprivation myopia (FDM). Investig. Ophthalmol. Vis. Sci. 2018, 59, 704.
  77. Lewis, R.J. Aggression, rank and power: Why hens (and other animals) do not always peck according to their strength. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2022, 377, 20200434.
  78. El Aidy, S.; Dinan, T.G.; Cryan, J.F. Gut Microbiota: The conductor in the orchestra of immune-neuroendocrine communication. Clin. Ther. 2015, 37, 954–967.
  79. Sarsero, J.P.; Merino, E.; Yanofsky, C. A Bacillus subtilis operon containing genes of unknown function senses tRNA(Trp) charging and regulates expression of the genes of tryptophan biosynthesis. Proc. Natl. Acad. Sci. USA 2000, 97, 2656–2661.
  80. Gollnick, P.; Babitzke, P.; Antson, A.; Yanofsky, C. Complexity in regulation of tryptophan biosynthesis in Bacillus subtilis. Ann. Rev. Genet. 2005, 39, 47–68.
  81. Bjerre, K.; Cantor, M.D.; Norgaard, J.V.; Poulsen, H.D.; Blaabjerg, K.; Canibe, N.; Jensen, B.B.; Stuer-Lauridsen, B.; Nielsen, B.; Derkx, P.M.. Development of Bacillus subtilis mutants to produce tryptophan in pigs. Biotechnol. Lett. 2017, 39, 289–295.
  82. Porter, R.J.; Phipps, A.J.; Gallagher, P.; Scott, A.; Stevenson, P.S.; O’Brien, J.T. Effects of acute tryptophan depletion on mood and cognitive functioning in older recovered depressed subjects. Am. J. Geriatr. Psychiatry 2005, 13, 607–615.
  83. van Veen, J.F.; van Vliet, I.M.; de Rijk, R.H.; van Pelt, J.; Mertens, B.; Fekkes, D.; Zitman, F.G. Tryptophan depletion affects the autonomic stress response in generalized social anxiety disorder. Psychoneuroendocrinology 2009, 34, 1590–1594.
  84. Duan, K.-M.; Ma, J.-H.; Wang, S.-Y.; Huang, Z.; Zhou, Y.; Yu, H. The role of tryptophan metabolism in postpartum depression. Metab. Brain Dis. 2018, 33, 647–660.
  85. Kaluzna-Czaplinska, J.; Gatarek, P.; Chirumbolo, S.; Chartrand, M.S.; Bjorklund, G. How important is tryptophan in human health? Crit. Rev. Food Sci. Nutr. 2019, 59, 72–88.
  86. Aune, T.M.; Pogue, S.L. Inhibition of tumor-cell growth by interferon-gamma is mediated by 2 distinct mechanisms dependent upon oxygen-tension-induction of tryptophan degradation and depletion of intracellular nicotinamide adenine-dinucleotide. J. Clin. Investig. 1989, 84, 863–875.
  87. Waider, J.; Araragi, N.; Gutknecht, L.; Lesch, K.-P. Tryptophan hydroxylase-2 (TPH2) in disorders of cognitive control and emotion regulation: A perspective. Psychoneuroendocrinology 2011, 36, 393–405.
  88. Rushen, J. The peck orders of chickens—How do they develop and why are they linear. Animal Behaviour. 1982, 30, 1129–1137.
  89. Shabalina, A.T. Dominance rank, fear scores and reproduction in cockerels. Br. Poult. Sci. 1984, 25, 297–301.
  90. D’Eath, R.B.; Keeling, L.J. Social discrimination and aggression by laying hens in large groups: From peck orders to social tolerance. Appl. Anim. Behav. Sci. 2003, 84, 197–212.
  91. Fox, A.S.; Kalin, N.H. A Translational neuroscience approach to understanding the development of social anxiety disorder and its pathophysiology. Am. J. Psychiatry 2014, 171, 1162–1173.
  92. Jupp, B.; Murray, J.E.; Jordan, E.R.; Xia, J.; Fluharty, M.; Shrestha, S.; Robbins, T.W.; Dalley, J.W. Social dominance in rats: Effects on cocaine self-administration, novelty reactivity and dopamine receptor binding and content in the striatum. Psychopharmacology 2016, 233, 579–589.
  93. Larrieu, T.; Sandi, C. Stress-induced depression: Is social rank a predictive risk factor? Bioessays 2018, 40, e1800012.
  94. Guhl, A.M.; Craig, J.V.; Mueller, C.D. Selective breeding for aggressiveness in chickens. Poult. Sci. 1960, 39, 970–980.
  95. Dennis, R.L.; Lay, D.C., Jr.; Cheng, H.W. Effects of early serotonin programming on behaviour and central monoamine concentrations in an avian model. Behav. Brain Res. 2013, 253, 290–296.
  96. Hollis, F.; Kabbaj, M. Social defeat as an animal model for depression. ILAR J. 2014, 55, 221–232.
  97. Abdel-Azeem, N.M. Do probiotics affect the behaviour of turkey poults? J. Vet. Med. Anim. Health 2013, 5, 144–148.
  98. Koolhaas, J.M.; Coppens, C.M.; de Boer, S.F.; Buwalda, B.; Meerlo, P.; Timmermans, P.J.A. The resident-intruder paradigm: A standardized test for aggression, violence and social stress. J. Vis. Exp. 2013, 4, e4367.
  99. Jager, A.; Maas, D.A.; Fricke, K.; de Vries, R.B.; Poelmans, G.; Glennon, J.C. Aggressive behaviour in transgenic animal models: A systematic review. Neurosci. Biobehav. Rev. 2018, 91, 198–217.
  100. Masis-Calvo, M.; Schmidtner, A.K.; de Moura Oliveira, V.E.; Grossmann, C.P.; de Jong, T.R.; Neumann, I.D. Animal models of social stress: The dark side of social interactions. Stress 2018, 21, 417–432.
  101. Cheng, H.W.; Eicher, S.D.; Chen, Y.; Singleton, P.; Muirt, W.M. Effect of genetic selection for group productivity and longevity on immunological and hematological parameters of chickens. Poult. Sci. 2001, 80, 1079–1086.
  102. Kriegseis, I.; Bessei, W.; Meyer, B.; Zentek, J.; Würbel, H.; Harlander-Matauschek, A. Feather-pecking response of laying hens to feather and cellulose-based rations fed during rearing. Poult. Sci. 2012, 91, 1514–1521.
  103. Bolhuis, J.E.; Ellen, E.D.; Van Reenen, C.G.; De Groot, J.; Ten Napel, J.; Koopmanschap, R.E.; Reilingh, G.D.; Uitdehaag, K.A.; Kemp, B.; Rodenburg, T.B. Effects of genetic group selection against mortality on behaviour and peripheral serotonin in domestic laying hens with trimmed and intact beaks. Physiol. Behav. 2009, 97, 470–475.
  104. Moffitt, T.E.; Brammer, G.L.; Caspi, A.; Fawcett, J.P.; Raleigh, M.; Yuwiler, A.; Silva, P. Whole blood serotonin relates to violence in an epidemiological study. Biol. Psychiatry 1998, 43, 446–457.
  105. Hercigonja Novkovic, V.; Rudan, V.; Pivac, N.; Nedic, G.; Muck-Seler, D. Platelet serotonin concentration in children with attention-deficit/hyperactivity disorder. Neuropsychobiology 2009, 59, 17–22.
  106. Rosado, B.; Garcia-Belenguer, S.; Palacio, J.; Chacon, G.; Villegas, A.; Alcalde, A.I. Serotonin transporter activity in platelets and canine aggression. Vet. J. 2010, 186, 104–105.
  107. Brown, G.L.; Goodwin, F.K.; Bunney, W.E., Jr. Human aggression and suicide: Their relationship to neuropsychiatric diagnoses and serotonin metabolism. Adv. Biochem. Psychopharmacol. 1982, 34, 287–307.
  108. Mann, J.J.; Brent, D.A.; Arango, V. The neurobiology and genetics of suicide and attempted suicide: A focus on the serotonergic system. Neuropsychopharmacology 2001, 24, 467–477.
  109. McDonald, M.D.; Gonzalez, A.; Sloman, K.A. Higher levels of aggression are observed in socially dominant toadfish treated with the selective serotonin reuptake inhibitor, fluoxetine. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2011, 153, 107–112.
  110. Pietraszek, M.H.; Takada, Y.; Yan, D.; Urano, T.; Serizawa, K.; Takada, A. Relationship between Serotonergic Measures in Periphery and the Brain of Mouse. Life Sci. 1992, 51, 75–82.
  111. Sarrias, M.J.; Martinez, E.; Celada, P.; Udina, C.; Alvarez, E.; Artigas, F. Plasma free 5HT and platelet 5HT in depression: Case-control studies and the effect of antidepressant therapy. Adv. Exp. Med. Biol. 1991, 294, 653–658.
  112. Yan, F.F.; Wang, W.C.; Cheng, H.W. Bacillus subtilis based probiotic improved bone mass and altered brain serotoninergic and dopaminergic systems in broiler chickens. J. Funct. Foods 2018, 49, 501–509.
  113. Wang, W.C.; Yan, F.F.; Hu, J.Y.; Amen, O.A.; Cheng, H.W. Supplementation of Bacillus subtilis-based probiotic reduces heat stress-related behaviours and inflammatory response in broiler chickens. J. Anim. Sci. 2018, 96, 1654–1666.