Abstract
Microorganisms represent the largest component of biodiversity in our world. For millions of years, prokaryotic microorganisms have functioned as a major selective force shaping eukaryotic evolution. Microbes that live inside and on animals outnumber the animals’ actual somatic and germ cells by an estimated 10-fold. Collectively, the intestinal microbiome represents a “forgotten organ,” functioning as an organ inside another that can execute many physiological responsibilities. The nature of primitive eukaryotes was drastically changed due to the association with symbiotic prokaryotes facilitating mutual coevolution of host and microbe. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. From termites and honey bees to ruminants and mammals, depending on novel biochemistries provided by the prokaryotic microbiome, the association helps to metabolize several nutrients that the host cannot digest and converting these into useful end products (such as short-chain fatty acids), a process, which has huge impact on the biology and homeostasis of metazoans. More importantly, in a direct and/or indirect way, the intestinal microbiota influences the assembly of gut-associated lymphoid tissue, helps to educate immune system, affects the integrity of the intestinal mucosal barrier, modulates proliferation and differentiation of its epithelial lineages, regulates angiogenesis, and modifies the activity of enteric as well as the central nervous system. Despite these important effects, the mechanisms by which the gut microbial community influences the host’s biology remain almost entirely unknown. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification between prokaryotes and eukaryotes, which encourage us to postulate: who is hosting whom?
The Microbiome and General Homeostasis
A common human propensity is to regard all microorganisms as “harmful,” in particular, equating bacteria to pathogenic germs. Nothing could be further from the truth. The number of beneficial bacterial species far exceeds the number of pathogenic species and many of the known bacteria are in fact useful or even indispensable for the continued existence of life on Earth. Prokaryotic microorganisms are widespread in all environments on Earth, establishing diverse interactions with many eukaryotic taxa (1, 2). The cooperative interactions between species (mutualism) have had a central role in the generation and maintenance of life on earth (3, 4). Prokaryotes and eukaryotes are involved in diverse forms of mutualism (5). Adaptive diversification is a process intrinsically tied to species interactions (6). Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. The endosymbiotic theory states that several key organelles of eukaryotes originated as symbioses between separate single-celled organisms (7). According to this theory, mitochondria and plastids (e.g., chloroplasts), and possibly other organelles, represent formerly free-living bacteria that were taken inside another cell as an endosymbiont, around 1.5 billion years ago (8). Molecular and biochemical evidence suggest that the mitochondrion developed from proteobacteria and the chloroplast from cyanobacteria (9). Numerous facultative heritable endosymbionts are reproductive manipulators (5). Nevertheless, many do not manipulate reproduction, so they are expected to confer fitness benefits to their hosts, as has been shown in several studies that report defense against natural enemies, tolerance to environmental stress, and increased fecundity (6). One example of such beneficial group of microorganisms is the incredibly complex and abundant ensemble of microbes that harbors in the gastrointestinal tract (GIT) of metazoans (10). The GIT is more densely populated with microorganisms than any other organ and is an interface where the microflora may have a pronounced impact on animal biology (11–13). More than 50 genera and at least 500–1,000 different species are distributed along the length of the GIT (10, 14, 15). The bacterial population of the human cecum and colon is numerically ~1013 cfu/g (10, 15, 16), comprising about 40–55% of solid stool matter and weights ~1 kg (17). Presumably, the assembly of gut microflora is regulated by elaborate and combinatorial host–microbial and microbial–microbial interactions predicated on principles refined over the course of evolution (16, 18, 19). Comparison of rodents raised without exposure to any microorganisms to those colonized with an assembly of microbiota revealed a wide range of host functions affected by indigenous microbial communities. For example, the microbiota directs the assembly of the gut-associated lymphoid tissue (20, 21), helps educate the immune system (22), affects the integrity of the intestinal mucosal barrier (23), modulates proliferation and differentiation of its epithelial lineages (24), regulates angiogenesis (21), modifies the activity of the enteric nervous system (25, 26), and plays a key role in extracting and processing nutrients consumed in the diet (27, 28). The microflora can metabolize proteins and protein degradation products, sulfur-containing compounds, and endogenous and exogenous glycoproteins (29, 30). Some organisms grow on intermediate products of fermentation such as H2, lactate, succinate, formate, and ethanol; converting these to end products including short-chain fatty acids, a process which has direct benefits on digestive physiology (31–33). In particular with diet composition, one must conclude that, metazoans literally “become what we eat.” So, any disorders in this fragile microbial ecosystem (disbacteriosis) may predispose the host to a whole range of chronic diseases and infections thereby affecting the production of food animals. On the other hand, over millions of years, animals have developed various means for supporting complex and dynamic consortia of microorganisms during their life cycle (34, 35). As with most complex ecosystems, it appears that the majority of these microbial species cannot be cultured when removed from the niches in their host animals (24). The fragile composition of the gut microflora can be affected by various factors such as age, diet, environment, stress, and medication (36, 37). Furthermore, many factors are involved in shaping gut microflora from infancy such as mode of delivery, type of infant feeding, hospitalization, prematurity, antibiotic use, and dietary nutrient composition (36, 38). Dietary ingredients have a profound effect on the composition of the gut microflora, which in turn regulates the physiology of all animals (19). As such, nutritional components of the diet are of critical importance not only for meeting the nutrient requirements of the host but also shaping the profile of the microbiome, which in turn will determine the balance between health and disease. As an example, several studies have shown the effect of diet composition in promoting insulin sensitivity, diabetes, cancer, and other metabolic disorders (39–44). Some researchers believe that the alarming increase in autoimmune diseases in the West may owe to a disruption in the ancient relationship between our bodies and a healthy microbiome (45). Thus, colonization of microbiomes in metazoans begins at birth, and is followed by progressive assembly of a complex and dynamic microbial society maintaining a perfect harmony or homeostasis (46). However, little is known about how they influence the normal development and physiology of hosts. A transcendent view of vertebrate biology therefore requires an understanding of the contributions of these indigenous microbial communities to host development and adult physiology.
The Microbiome and the Immune System
Today, the fields of immunology, microbiology, and nutrition converge in an astonishing way (47). Balanced gastrointestinal microflora and immune-stimulation are major functional effects attributed to beneficial bacteria (48–50). In this context, a short window of time during birth exists that enables the colonization of symbiotic bacteria to all mucosal surfaces, which may modify the future immune phenotype of the host (51–53). Perhaps, a delayed microbial colonization of the gut mucosa, the largest immune organ of the body, could cause significant changes in the immune system possibly having long term impacts on systemic immunity (54–60). For instance, some effects of the microbiome are mediated through immune regulation, particularly through balanced control of pro-inflammatory and anti-inflammatory cytokines (61, 62). Moreover, several animal and human studies have provided unequivocal evidence that specific bacterial strains are capable of stimulating multiple aspects of innate immunity (63–67) as well as to increase humoral immunity (68–70). Very interestingly, through a process of “cross talk” with the mucosal immune system, the microbiota negotiates mutual growth, survival, and inflammatory control of the intestinal ecosystem and pathogen control (71–75).
The Microbiome–Gut–Brain Axis
Gut bacteria produce hundreds of neurochemicals that the brain uses to regulate basic physiological as well as mental processes such as learning, memory, and mood variations (76, 77). Today, it has been recognized that the microbiome–gut–brain axis influences brain chemistry and behavior independently of the autonomic nervous system, gastrointestinal-specific neurotransmitters, or inflammation (78). The ability of the microflora to synthesize neuroactive compounds such as acetylcholine, dihydroxyphenylacetic acid, l-3,4-dihydroxyphenylalanine, dopamine-4-O-sulfate, epinephrine, γ-aminobutyric acid, histamine, norepinephrine, serotonine, tyramine, among others, provides some microbial endocrinology-based mechanism that may help to explain some of the mechanisms, both immunological and neurophysiological components, by which the microbiome modulates the biology of their host (79). The fact that bacteria not only produce but also respond to neurochemicals produced by the host has led to the creation of a new field of study, microbial endocrinology, providing convincing evidence that cell-to-cell signaling in metazoans may be due to late horizontal gene transfer from bacteria (80). As an evidence of this astonishing link between prokaryotes and their hosts, some probiotic strains have been shown to reduce anxiety and depression by lowering the levels of corticosterone (81), as well as helping program some aspects of brain development in neonates (82–84). There is a lot of truth in the old saying “thinking with your gut,” since the enteric nervous system, known as the “second brain” contains more neurons than the peripheral nervous system (79). More recently, various studies have also linked some gut microflora with autism (85–88). Conversely, just as gut bacteria affect the brain, the brain can also exert profound influences on the gut microbiome, with feedback effects on behavior. This may help explain why people with inflammatory syndromes such as Crohn’s disease, ulcerative colitis, or irritable bowel syndrome are also plagued by anxiety and depression (89–91). High and chronic levels of stress hormones such as epinephrine and norepinephrine have been shown to increase virulence and pathogenicity of several pathogenic enterobacteria (92–95). This neurochemical-mediated “two-way street” is one of the principles that undergirds the microbial endocrinology construct that unify animal and plant kingdoms with the same origin, since for example, stress-related neuroendocrine hormone family of catecholamines has also been demonstrated in all forms of life on earth (79).
Who is Hosting Whom?
Wolbachia are common intracellular bacteria that are found in arthropods and nematodes (5). It is one of the world’s most common parasitic microbes and is possibly the most common reproductive parasite in the biosphere (96). Its interactions with its hosts are often complex, and in some cases have evolved to be mutualistic rather than parasitic. Some host species cannot reproduce, or even survive, without Wolbachia infection (97). These proteobacteria endosymbionts are transmitted vertically through host eggs and alter host biology in diverse ways, including the induction of reproductive manipulations, such as feminization, parthenogenesis, male killing, and sperm-egg incompatibility and they can also move horizontally across species boundaries, resulting in a widespread and global distribution in diverse invertebrate hosts (98).
Prokaryotes also have developed a sophisticated system of stimulus, communication, and response (quorum sensing) that many species of bacteria use to coordinate gene expression that coordinate certain behaviors such as biofilm formation, virulence, and antibiotic resistance, based on the local density of the bacterial population (99–102). Quorum sensing occurs within a single bacterial species as well as between diverse species, and the cells of the host, serving as a simple indicator of population density or the diffusion rate of the cell’s immediate environment (103–107).
At a higher biological level, there is clear evidence that even some parasites can be also excellent manipulators of their host. It is remarkable that when two parasite species are manipulators and have different definitive hosts, there is a potential for conflict between them. Selection may then exist for either avoiding hosts infected with conflicting parasites, or for hijacking, i.e., competitive processes to gain control of the intermediate host (108). The evidence for both phenomena depends largely on the study of the relative competitive abilities of parasites within their common intermediate host. Adaptive host manipulation hypothesis is usually supported by case studies on trophically transmitted heteroxenous endoparasites. Trematodes and cestodes are among efficient manipulators of fish, their common intermediate hosts. Reviewed experimental data suggest that heteroxenous parasites manipulate their host mainly through impaired defense behavior, e.g., impairing shoaling in fish. Alternatively, monoxenous parasites facilitate shoaling that is profitable for both parasites and hosts (109). Coordination of modified host behavior with the parasite life cycle, both temporal and spatial, is the most convincing criterion of the adaptive value of host manipulation (110). In human beings, seropositivity of the obligate intracellular protozoan parasite, T. gondii is related to various mental health disorders including schizophrenia, suicide attempt, depression, and other neuropsychiatric diseases (111). Depressive symptoms have been linked to interferon-γ (IFN-γ) blocking T. gondii growth by inducing indoleamine-2,3-dioxygenase (IDO) activation and tryptophan depletion, which results in a decrease of serotonin production in the brain (112).
Final Remarks
The interest in digestive physiology and the role of microorganisms has generated data whereby human and animal well being can be enhanced and the risk of disease reduced. New molecular techniques that allow more accurate assessment of the flora composition are resulting in improved strategies for elucidating mechanisms. The research field of beneficial microorganisms to animals and humans (probiotics) has been aimed at modulating the intestinal microflora and current research is still heavily biased toward gastrointestinal applications for probiotics, such as chronic constipation (113), chronic diarrhea (114), inflammatory bowel disease (115), irritable bowel syndrome (116), and food allergy (117), the possibilities for impacting many areas of health are numerous. However, other parts of the body containing endogenous microflora or problems relating to the immune system may also be candidates for probiotic therapy. A few researchers have already shown that probiotics have potential for human health issues such as vaginal candidiosis (118), dental caries (119), allergies (120), autoimmune diseases (121), urogenital infections (122), atopic diseases (69), rheumatoid arthritis (26), and respiratory infections (68). It has been said that “nothing is new under the sun.” There are no new or novel discoveries in this review that have not been clearly described previously by numerous scientists. Rather, the purpose of this manuscript is simply trying to put some of the puzzle pieces together. When we ponder and contemplate the astonishing and remarkable roles that prokaryotes have on host metabolism, immune function, gene expression, reproduction, and behavior of metazoans, I wonder who is, in reality, hosting whom?
Statements
Conflict of interest
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
1
BronsteinJLAlarcónRGeberM. The evolution of plant-insect mutualisms. New Phytol (2006) 172:412–28.10.1111/j.1469-8137.2006.01864.x
2
GnadFFornerFZielinskaDFBirneyEGunawardenaJMannM. Evolutionary constraints of phosphorylation in eukaryotes, prokaryotes, and mitochondria. Mol Cell Proteomics (2010) 9:2642–53.10.1074/mcp.M110.001594
3
KikuchiYHosokawaTNikohNMengX-YKamagataYFukatsuT. Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biol (2009) 7:2.10.1186/1741-7007-7-2
4
JonesEOWhiteABootsM. The evolution of host protection by vertically transmitted parasites. Proc Biol Sci (2011) 2010:863–70.10.1098/rspb.2010.1397
5
SaridakiABourtzisK. Wolbachia: more than just a bug in insects genitals. Curr Opin Microbiol (2010) 13:67–72.10.1016/j.mib.2009.11.005
6
XieJVilchezIMateosM. Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS One (2010) 5:e12149.10.1371/journal.pone.0012149
7
Degli EspostiMChouaiaBComandatoreFCrottiESasseraDLievensPM-Jet alEvolution of mitochondria reconstructed from the energy metabolism of living bacteria. PLoS One (2014) 9:e96566.10.1371/journal.pone.0096566
8
GibsonCMHunterMS. Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecol Lett (2010) 13:223–34.10.1111/j.1461-0248.2009.01416.x
9
MackiewiczPBodylAGagatP. Possible import routes of proteins into the cyanobacterial endosymbionts/plastids of Paulinella chromatophora. Theory Biosci (2012) 131:1–18.10.1007/s12064-011-0147-7
10
NeishAS. Microbes in gastrointestinal health and disease. Gastroenterology (2009) 136:65–80.10.1053/j.gastro.2008.10.080
11
YeganiMKorverD. Factors affecting intestinal health in poultry. Poult Sci (2008) 87:2052–63.10.3382/ps.2008-00091
12
MaslowskiKMMackayCR. Diet, gut microbiota and immune responses. Nat Immunol (2010) 12:5–9.10.1038/ni0111-5
13
MussoGGambinoRCassaderM. Obesity, diabetes, and gut microbiota: the hygiene hypothesis expanded?Diabetes Care (2010) 33:2277–84.10.2337/dc10-0556
14
SchiffrinEBlumS. Interactions between the microbiota and the intestinal mucosa. Eur J Clin Nutr (2002) 56:S60–4.10.1038/sj.ejcn.1601489
15
SharmaRYoungCNeuJ. Molecular modulation of intestinal epithelial barrier: contribution of microbiota. J Biomed Biotechnol (2010) 2010:305879.10.1155/2010/305879
16
XuJGordonJI. Honor thy symbionts. Proc Natl Acad Sci U S A (2003) 100:10452–9.10.1073/pnas.1734063100
17
BlaserMJ. Who are we? Indigenous microbes and the ecology of human diseases. EMBO Rep (2006) 7:956.10.1038/sj.embor.7400812
18
XuJMahowaldMALeyRELozuponeCAHamadyMMartensECet alEvolution of symbiotic bacteria in the distal human intestine. PLoS Biol (2007) 5:e156.10.1371/journal.pbio.0050156
19
FrauneSBoschTC. Why bacteria matter in animal development and evolution. Bioessays (2010) 32:571–80.10.1002/bies.200900192
20
MartinRNautaABen AmorKKnippelsLMKnolJGarssenJ. Early life: gut microbiota and immune development in infancy. Benef Microbes (2010) 1:367–82.10.3920/BM2010.0027
21
SekirovIRussellSLAntunesLCMFinlayBB. Gut microbiota in health and disease. Physiol Rev (2010) 90:859–904.10.1152/physrev.00045.2009
22
McFall-NgaiM. Adaptive immunity: care for the community. Nature (2007) 445:153–153.10.1038/445153a
23
DuerkopBAVaishnavaSHooperLV. Immune responses to the microbiota at the intestinal mucosal surface. Immunity (2009) 31:368–76.10.1016/j.immuni.2009.08.009
24
MoranNA. Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci U S A (2007) 104(Suppl 1):8627–33.10.1073/pnas.0611659104
25
ShermanPMOssaJCJohnson-HenryK. Unraveling mechanisms of action of probiotics. Nutr Clin Pract (2009) 24:10–4.10.1177/0884533608329231
26
Tlaskalová-HogenováHStepánkováRKozákováHHudcovicTVannucciLTuckováLet alThe role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell Mol Immunol (2011) 8:110–20.10.1038/cmi.2010.67
27
BergmanE. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev (1990) 70:567–90.
28
WalterJBrittonRARoosS. Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm. Proc Natl Acad Sci U S A (2011) 108(Suppl 1):4645–52.10.1073/pnas.1000099107
29
FullerRBrookerB. Lactobacilli which attach to the crop epithelium of the fowl. Am J Clin Nutr (1974) 27:1305–12.
30
QiuRCroomJAliRBallouASmithCAshwellCet alDirect fed microbial supplementation repartitions host energy to the immune system. J Anim Sci (2012) 90:2639–51.10.2527/jas.2011-4611
31
TellezGHigginsSDonoghueAHargisB. Digestive physiology and the role of microorganisms. J Appl Poult Res (2006) 15:136–44.10.1093/japr/15.1.136
32
TellezGPixleyCWolfendenRLaytonSHargisB. Probiotics/direct fed microbials for Salmonella control in poultry. Food Res Intern (2012) 45:628–33.10.1016/j.foodres.2011.03.047
33
DassNJohnABassilACrumbleyCSheheeWMaurioFet alThe relationship between the effects of short-chain fatty acids on intestinal motility in vitro and GPR43 receptor activation. Neurogastroenterol Motil (2007) 19:66–74.10.1111/j.1365-2982.2006.00853.x
34
DaleCMoranNA. Molecular interactions between bacterial symbionts and their hosts. Cell (2006) 126:453–65.10.1016/j.cell.2006.07.014
35
DethlefsenLMcFall-NgaiMRelmanDA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature (2007) 449:811–8.10.1038/nature06245
36
ChoctM. Managing gut health through nutrition. Br Poult Sci (2009) 50:9–15.10.1080/00071660802538632
37
BäckhedF. Programming of host metabolism by the gut microbiota. Ann Nutr Metab (2011) 58(Suppl 2):44–52.10.1159/000328042
38
KauALAhernPPGriffinNWGoodmanALGordonJI. Human nutrition, the gut microbiome and the immune system. Nature (2011) 474:327–36.10.1038/nature10213
39
CaniPDBibiloniRKnaufCWagetANeyrinckAMDelzenneNMet alChanges in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes (2008) 57:1470–81.10.2337/db07-1403
40
CaniPDDelzenneNM. The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des (2009) 15:1546–58.10.2174/138161209788168164
41
SalehMElsonCO. Experimental inflammatory bowel disease: insights into the host-microbiota dialog. Immunity (2011) 34:293–302.10.1016/j.immuni.2011.03.008
42
ElsonCOCongY. Host-microbiota interactions in inflammatory bowel disease. Gut Microbes (2012) 3:332–44.10.4161/gmic.20228
43
ShenJObinMSZhaoL. The gut microbiota, obesity and insulin resistance. Mol Aspects Med (2012) 34(1):39–58.10.2119/molmed.2012.00111
44
TagliabueAElliM. The role of gut microbiota in human obesity: recent findings and future perspectives. Nutr Metab Cardiovasc Dis (2012) 23(3):160–8.10.1016/j.numecd.2012.09.002
45
SalzmanNH. Microbiota-immune system interaction: an uneasy alliance. Curr Opin Microbiol (2011) 14:99–105.10.1016/j.mib.2010.09.018
46
Di MauroANeuJRiezzoGRaimondiFMartinelliDFrancavillaRet alGastrointestinal function development and microbiota. Ital J Pediatr (2013) 39:1–7.10.1186/1824-7288-39-15
47
GillNWlodarskaMFinlayBB. The future of mucosal immunology: studying an integrated system-wide organ. Nat Immunol (2010) 11:558–60.10.1038/ni0710-558
48
HammesWPHertelC. Research approaches for pre-and probiotics: challenges and outlook. Food Res Intern (2002) 35:165–70.10.1016/S0963-9969(01)00178-8
49
ParvezSMalikKAh KangSKimH-Y. Probiotics and their fermented food products are beneficial for health. J Appl Microbiol (2006) 100:1171–85.10.1111/j.1365-2672.2006.02963.x
50
ParrachoHMcCartneyALGibsonGR. Probiotics and prebiotics in infant nutrition. Proc Nutr Soc (2007) 66:405–11.10.1017/S0029665107005678
51
AlmqvistCCnattingiusSLichtensteinPLundholmC. The impact of birth mode of delivery on childhood asthma and allergic diseases – a sibling study. Clin Exp Allergy (2012) 42:1369–76.10.1111/j.1365-2222.2012.04021.x
52
MartinDH. The microbiota of the vagina and its influence on women’s health and disease. Am J Med Sci (2012) 343:2.10.1097/MAJ.0b013e31823ea228
53
HansenCHMetzdorffSBHansenA. Customizing laboratory mice by modifying gut microbiota and host immunity in an early “window of opportunity”. Gut microbes (2013) 4:241–5.10.4161/gmic.23999
54
StevcevaLAbimikuAFranchiniG. Targeting the mucosa: genetically engineered vaccines and mucosal immune responses. Genes Immun (2000) 1:308–15.10.1038/sj.gene.6363680
55
SalminenSGibsonGMcCartneyAIsolauriE. Influence of mode of delivery on gut microbiota composition in seven year old children. Gut (2004) 53:1388–9.10.1136/gut.2004.041640
56
MshvildadzeMNeuJMaiV. Intestinal microbiota development in the premature neonate: establishment of a lasting commensal relationship?Nutr Rev (2008) 66:658–63.10.1111/j.1753-4887.2008.00119.x
57
ThavagnanamSFlemingJBromleyAShieldsMCardwellC. A meta-analysis of the association between caesarean section and childhood asthma. Clin Exp Allergy (2008) 38:629–33.10.1111/j.1365-2222.2007.02780.x
58
NeuJRushingJ. Cesarean versus vaginal delivery: long term infant outcomes and the hygiene hypothesis. Clin Perinatol (2011) 38:321–31.10.1016/j.clp.2011.03.008
59
ColladoMCCernadaMBaüerlCVentoMPérez-MartínezG. Microbial ecology and host-microbiota interactions during early life stages. Gut microbes (2012) 3:352–65.10.4161/gmic.21215
60
GuibasGVMoschonisGXepapadakiPRoumpedakiEAndroutsosOManiosYet alConception via in vitro fertilization and delivery by caesarean section are associated with paediatric asthma incidence. Clin Exp Allergy (2013) 43:1058–66.10.1111/cea.12152
61
BraatHvan den BrandeJvan TolEHommesDPeppelenboschMvan DeventerS. Lactobacillus rhamnosus induces peripheral hyporesponsiveness in stimulated CD4+ T cells via modulation of dendritic cell function. Am J Clin Nutr (2004) 80:1618–25.
62
BorchersATSelmiCMeyersFJKeenCLGershwinME. Probiotics and immunity. J Gastroenterol (2009) 44:26–46.10.1007/s00535-008-2296-0
63
Alvarez-OlmosMIOberhelmanRA. Probiotic agents and infectious diseases: a modern perspective on a traditional therapy. Clin Infect Dis (2001) 32:1567–76.10.1086/320518
64
ReveneauNGeoffroyM-CLochtCChagnaudPMercenierA. Comparison of the immune responses induced by local immunizations with recombinant Lactobacillus plantarum producing tetanus toxin fragment C in different cellular locations. Vaccine (2002) 20:1769–77.10.1016/S0264-410X(02)00027-0
65
FarnellMDonoghueADe Los SantosFSBlorePHargisBTellezGet alUpregulation of oxidative burst and degranulation in chicken heterophils stimulated with probiotic bacteria. Poult Sci (2006) 85:1900–6.10.1093/ps/85.11.1900
66
FengTElsonC. Adaptive immunity in the host-microbiota dialog. Mucosal Immunol (2010) 4:15–21.10.1038/mi.2010.60
67
JounaiKIkadoKSugimuraTAnoYBraunJFujiwaraD. Spherical lactic acid bacteria activate plasmacytoid dendritic cells immunomodulatory function via TLR9-dependent crosstalk with myeloid dendritic cells. PLoS One (2012) 7:e32588.10.1371/journal.pone.0032588
68
ArvolaTLaihoKTorkkeliSMykkänenHSalminenSMaunulaLet alProphylactic Lactobacillus GG reduces antibiotic-associated diarrhea in children with respiratory infections: a randomized study. Pediatrics (1999) 104:e64–64.10.1542/peds.104.5.e64
69
KalliomakiMSalminenSArvilommiHKeroPKoskinenPIsolauriEet alProbiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet (2001) 357:1076–9.10.1016/S0140-6736(00)04259-8
70
OuwehandAIsolauriESalminenS. The role of the intestinal microflora for the development of the immune system in early childhood. Eur J Nutr (2002) 41:I32–7.10.1007/s00394-002-1105-4
71
HigginsJHigginsSVicenteJWolfendenATellezGHargisB. Temporal effects of lactic acid bacteria probiotic culture on Salmonella in neonatal broilers. Poult Sci (2007) 86:1662–6.10.1093/ps/86.8.1662
72
HigginsJPAndreatti FilhoRLHigginsSEWolfendenADTéllezGHargisBM. Evaluation of Salmonella-lytic properties of bacteriophages isolated from commercial broiler houses. Avian Dis (2008) 52:139–42.10.1637/8017-050807-ResNote
73
HigginsJHigginsSWolfendenAHendersonSTorres-RodriguezAVicenteJet alEffect of lactic acid bacteria probiotic culture treatment timing on Salmonella Enteritidis in neonatal broilers. Poult Sci (2010) 89:243–7.10.3382/ps.2009-00436
74
VicenteJHigginsSHargisBTellezG. Effect of poultry guard litter amendment on horizontal transmission of Salmonella enteritidis in broiler chicks. Int J Poult Sci (2007) 6:314–7.10.3923/ijps.2007.314.317
75
LaytonSLXochitlH-VShivaramaiahCJorgeXAnitaMJuan DavidLet alThe effect of a Lactobacillus-based probiotic for the control of necrotic enteritis in broilers. Food Nutr Sci (2013) 4:1–7.10.4236/fns.2013.411A001
76
McFall-NgaiMJ. Unseen forces: the influence of bacteria on animal development. Dev Biol (2002) 242:1–14.10.1006/dbio.2001.0522
77
BercikPDenouECollinsJJacksonWLuJJuryJet alThe intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology (2011) 141:599–609.10.1053/j.gastro.2011.04.052
78
BercikPParkASinclairDKhoshdelALuJHuangXet alThe anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterol Motil (2011) 23:1132–9.10.1111/j.1365-2982.2011.01796.x
79
LyteM. Probiotics function mechanistically as delivery vehicles for neuroactive compounds: microbial endocrinology in the design and use of probiotics. Bioessays (2011) 33:574–81.10.1002/bies.201100024
80
IyerLMAravindLCoonSLKleinDCKooninEV. Evolution of cell-cell signaling in animals: did late horizontal gene transfer from bacteria have a role?. Trends Genet (2004) 20:292–299.
81
RatcliffeEMFarrarNRFoxEA. Development of the vagal innervation of the gut: steering the wandering nerve. Neurogastroenterol Motil (2011) 23:898–911.10.1111/j.1365-2982.2011.01764.x
82
LallèsJ-PBosiPSmidtHStokesCR. Nutritional management of gut health in pigs around weaning. Proc Nutr Soc (2007) 66:260–8.10.1017/S0029665107005484
83
AlySMAbdel-Galil AhmedYAbdel-Aziz GhareebAMohamedMF. Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of Tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol (2008) 25:128–36.10.1016/j.fsi.2008.03.013
84
KonturekPBrzozowskiTKonturekS. Stress and the gut: pathophysiology, clinical consequences, diagnostic approach and treatment options. J Physiol Pharmacol (2011) 62:591–9.
85
MacFabeDF. Short-chain fatty acid fermentation products of the gut microbiome: implications in autism spectrum disorders. Microb Ecol Health Dis (2012) 23:19260.10.3402/mehd.v23i0.19260
86
MidtvedtT. The gut: a triggering place for autism-possibilities and challenges. Microb Ecol Health Dis (2012) 23:18982.10.3402/mehd.v23i0.18982
87
KangD-WParkJGIlhanZEWallstromGLaBaerJAdamsJBet alReduced incidence of Prevotella and other fermenters in intestinal microflora of autistic children. PLoS One (2013) 8:e68322.10.1371/journal.pone.0068322
88
WangLChristophersenCTSorichMJGerberJPAngleyMTConlonMA. Increased abundance of Sutterella spp. and Ruminococcus torques in feces of children with autism spectrum disorder. Mol Autism (2013) 4:42.10.1186/2040-2392-4-42
89
GoossensDJonkersDStobberinghEBogaardAvan den RusselMStockbruggerR. Probiotics in gastroenterology: indications and future perspectives. Scand J Gastroenterol Suppl (2003) 38:15–6.10.1080/00855920310002645
90
ElsonCOCongYQiFHershbergRMTarganSR. Molecular approaches to the role of the microbiota in inflammatory bowel disease. Ann N Y Acad Sci (2006) 1072:39–51.10.1196/annals.1326.010
91
WuH-JWuE. The role of gut microbiota in immune homeostasis and autoimmunity. Gut microbes (2012) 3:4–14.10.4161/gmic.19320
92
KaravolosMSpencerHBulmerDThompsonAWinzerKWilliamsPet alAdrenaline modulates the global transcriptional profile of Salmonella revealing a role in the antimicrobial peptide and oxidative stress resistance responses. BMC Genomics (2008) 9:458.10.1186/1471-2164-9-458
93
KaravolosMHBulmerDMSpencerHRampioniGSchmalenIBakerSet alSalmonella Typhi sense host neuroendocrine stress hormones and release the toxin haemolysin E. EMBO Rep (2011) 12:252–8.10.1038/embor.2011.4
94
MoreiraCGWeinshenkerDSperandioV. QseC mediates Salmonella enterica serovar Typhimurium virulence in vitro and in vivo. Infect Immun (2010) 78:914–26.10.1128/IAI.01038-09
95
MoreiraCGSperandioV. Interplay between the QseC and QseE bacterial adrenergic sensor kinases in Salmonella enterica serovar Typhimurium pathogenesis. Infect Immun (2012) 80:4344–53.10.1128/IAI.00803-12
96
KoutsovoulosGMakepeaceBTanyaVNBlaxterM. Palaeosymbiosis revealed by genomic fossils of Wolbachia in a strongyloidean nematode. PLoS Genet (2014) 10:e1004397.10.1371/journal.pgen.1004397
97
GentyL-MBouchonDRaimondMBertauxJ. Wolbachia infect ovaries in the course of their maturation: last minute passengers and priority travellers?PLoS One (2014) 9:e94577.10.1371/journal.pone.0094577
98
BrelsfoardCTsiamisGFalchettoMGomulskiLMTelleriaEAlamUet alPresence of extensive Wolbachia symbiont insertions discovered in the genome of its host Glossina morsitans morsitans. PLoS Negl Trop Dis (2014) 8:e2728.10.1371/journal.pntd.0002728
99
De KievitTRIglewskiBH. Bacterial quorum sensing in pathogenic relationships. Infect Immun (2000) 68:4839–49.10.1128/IAI.68.9.4839-4849.2000
100
DonlanRM. Biofilms: microbial life on surfaces. Emerg Infect Dis (2002) 8:881–90.10.3201/eid0809.020063
101
LadeHPaulDKweonJH. Quorum quenching mediated approaches for control of membrane biofouling. Int J Biol Sci (2014) 10:547.10.7150/ijbs.9028
102
RyallBCarraraMZlosnikJEBehrendsVLeeXWongZet alThe mucoid switch in Pseudomonas aeruginosa represses quorum sensing systems and leads to complex changes to stationary phase virulence factor regulation. PLoS One (2014) 9:e96166.10.1371/journal.pone.0096166
103
McFall-NgaiMJ. Identifying “prime suspects”: symbioses and the evolution of multicellularity. Comp Biochem Physiol B Biochem Mol Biol (2001) 129:711–23.10.1016/S1096-4959(01)00406-7
104
WilliamsP. Bacillus subtilis: a shocking message from a probiotic. Cell Host Microbe (2007) 1:248–9.10.1016/j.chom.2007.05.010
105
JabbariSHeapJTKingJR. Mathematical modelling of the sporulation-Initiation network in Bacillus subtilis revealing the dual role of the putative quorum-sensing signal molecule PhrA. Bull Math Biol (2011) 73:181–211.10.1007/s11538-010-9530-7
106
DogsaIChoudharyKSMarseticZHudaiberdievSVeraRPongorSet alComQXPA quorum sensing systems may not be unique to Bacillus subtilis: a census in prokaryotic genomes. PLoS One (2014) 9:e96122.10.1371/journal.pone.0096122
107
HartmannARothballerMHenseBASchröderP. Bacterial quorum sensing compounds are important modulators of microbe-plant interactions. Front Plant Sci (2014) 5:131.10.3389/fpls.2014.00131
108
PoulinR. Manipulation of host behaviour by parasites: a weakening paradigm?Proc Biol Sci (2000) 267:787–92.10.1098/rspb.2000.1072
109
JonesSR. The occurrence and mechanisms of innate immunity against parasites in fish. Dev Comp Immunol (2001) 25:841–52.10.1016/S0145-305X(01)00039-8
110
BerenreiterováMFlegrJKubenaAANemecP. The distribution of Toxoplasma gondii cysts in the brain of a mouse with latent toxoplasmosis: implications for the behavioral manipulation hypothesis. PLoS One (2011) 6:e28925.10.1371/journal.pone.0028925
111
OkusagaOLangenbergPSleemiAVaswaniDGieglingIHartmannAMet alToxoplasma gondii antibody titers and history of suicide attempts in patients with schizophrenia. Schizophr Res (2011) 133:150–5.10.1016/j.schres.2011.08.006
112
YagmurFYazarSTemelHOCavusogluM. May Toxoplasma gondii increase suicide attempt-preliminary results in Turkish subjects?Forensic Sci Int (2010) 199:15–7.10.1016/j.forsciint.2010.02.020
113
BuL-NChangM-HNiY-HChenH-LChengC-C. Lactobacillus casei rhamnosus Lcr35 in children with chronic constipation. Pediatr Int (2007) 49:485–90.10.1111/j.1442-200X.2007.02397.x
114
RolfeRD. The role of probiotic cultures in the control of gastrointestinal health. J Nutr (2000) 130:396S–402S.
115
JonkersDStockbrüggerR. Probiotics and inflammatory bowel disease. J R Soc Med (2003) 96:167–71.10.1258/jrsm.96.4.167
116
QuigleyEM. Probiotics and irritable bowel syndrome. Biosci Microflora (2009) 28:119–24.10.12938/bifidus.28.119
117
KirjavainenPApostolouESalminenSIsolauriE. New aspects of probiotics-a novel approach in the management of food allergy. Allergy (2001) 54:909–15.10.1034/j.1398-9995.1999.00103.x
118
HawesSEHillierSLBenedettiJStevensCEKoutskyLAWølner- HanssenPet alHydrogen peroxide-producing lactobacilli and acquisition of vaginal infections. J Infect Dis (1996) 174:1058–63.10.1093/infdis/174.5.1058
119
GrossELLeysEJGasparovichSRFirestoneNDSchwartzbaumJAJaniesDAet alBacterial 16S sequence analysis of severe caries in young permanent teeth. J Clin Microbiol (2010) 48:4121–8.10.1128/JCM.01232-10
120
Dominguez-BelloMGBlaserMJ. Do you have a probiotic in your future?Microbes Infect (2008) 10:1072.10.1016/j.micinf.2008.07.036
121
BachJ-F. Infections and autoimmune diseases. J Autoimmun (2005) 25:74.10.1016/j.jaut.2005.09.024
122
ReidGBruceA. Urogenital infections in women: can probiotics help?Postgrad Med J (2003) 79:428–32.10.1136/pmj.79.934.428
Summary
Keywords
microbiome, prokaryotes, eukaryotes, microbial endocrinology, probiotics, digestive physiology, enteric nervous system
Citation
Tellez G (2014) Prokaryotes Versus Eukaryotes: Who is Hosting Whom?. Front. Vet. Sci. 1:3. doi: 10.3389/fvets.2014.00003
Received
07 May 2014
Accepted
23 June 2014
Published
14 October 2014
Volume
1 - 2014
Edited by
James Allen Byrd, United States Department of Agriculture, USA
Reviewed by
Jason Kindrachuk, National Institutes of Health, USA; Andrew Patterson, The Pennsylvania State University, USA
Copyright
© 2014 Tellez.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Guillermo Tellez, The John Kirkpatrick Skeeles Poultry Health Laboratory, Department of Poultry Science, The Center of Excellence for Poultry Science, University of Arkansas, 1260 West, Maple, POSC 0-114, Fayetteville, AR 72701, USA e-mail: gtellez@uark.edu
This article was submitted to Veterinary Infectious Diseases, a section of the journal Frontiers in Veterinary Science.
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.