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Metabolism, bioenergetics and thermal physiology: influences of the human intestinal microbiota

  • Lawrence E. Armstrong (a1), Douglas J. Casa (a2) and Luke N. Belval (a2)


The micro-organisms which inhabit the human gut (i.e. the intestinal microbiota) influence numerous human biochemical pathways and physiological functions. The present review focuses on two questions, ‘Are intestinal microbiota effects measurable and meaningful?’ and ‘What research methods and variables are influenced by intestinal microbiota effects?’. These questions are considered with respect to doubly labelled water measurements of energy expenditure, heat balance calculations and models, measurements of RMR via indirect calorimetry, and diet-induced energy expenditure. Several lines of evidence suggest that the intestinal microbiota introduces measurement variability and measurement errors which have been overlooked in research studies involving nutrition, bioenergetics, physiology and temperature regulation. Therefore, we recommend that present conceptual models and research techniques be updated via future experiments, to account for the metabolic processes and regulatory influences of the intestinal microbiota.


Corresponding author

* Corresponding author: Lawrence E. Armstrong, email


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1. Savage, DC (1977) Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 1, 107133.
2. O’Hara, AM & Shanahan, F (2006) The gut flora as a forgotten organ. EMBO Rep 7, 688693.
3. Gosalbes, MJ, Durbán, A, Pignatelli, M, et al. (2011) Metatranscriptomic approach to analyze the functional human gut microbiota. PLoS ONE 6, e17447.
4. Li, J, Jia, H, Cai, X, et al. (2014) An integrated catalog of reference genes in the human gut microbiome. Nature Biotech 32, 834841.
5. Ehrlich, SD (2010) Metagenomics of the intestinal microbiota: potential applications. Gastroenterol Clin Biol 34, S23S28.
6. Sender, R, Fuchs, S & Milo, R (2016) Revised estimates for the number of human and bacteria cells in the body. PLoS Biol 14, e1002533.
7. Bordenstein, SR & Theis, KR (2015) Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol 13, e1002226.
8. Theis, KR, Dheilly, NM, Klassen, JL, et al. (2016) Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1, e0002816.
9. Hooper, LV, Littman, DR & Macpherson, AJ (2012) Interactions between the microbiota and the immune system. Science 336, 12681273.
10. Sharon, G, Garg, N, Debelius, J, et al. (2014) Specialized metabolites from the microbiome in health and disease. Cell Metab 20, 719730.
11. Koropatkin, NM, Cameron, EA & Martens, EC (2012) How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10, 323335.
12. Koh, A, De Vadder, F, Kovatcheva-Datchary, P, et al. (2016) From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165, 13321345.
13. Ramakrishna, BS (2013) Role of the gut microbiota in human nutrition and metabolism. J Gastroenterol Hepatol 28, 917.
14. Kohl, KD & Carey, HV (2016) A place for host-microbe symbiosis in the comparative physiologist’s toolbox. J Exp Biol 219, 34963504.
15. Bauer, E, Laczny, CC, Magnusdottir, S, et al. (2015) Phenotypic differentiation of gastrointestinal microbes is reflected in their encoded metabolic repertoires. Microbiome 3, 55.
16. Dumas, ME (2011) The microbial–mammalian metabolic axis: beyond simple metabolism. Cell Metab 13, 489490.
17. Flint, HJ, Duncan, SH, Scott, KP, et al. (2007) Interactions and competition within the microbial community of the human colon: links between diet and health. Environ Microbiol 9, 11011111.
18. Leone, V, Gibbons, SM, Martinez, K, et al. (2015) Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe 17, 681689.
19. Panda, S (2016) Circadian physiology of metabolism. Science 354, 10081015.
20. Scholz-Ahrens, KE & Schrezenmeir, J (2007) Inulin and oligofructose and mineral metabolism: the evidence from animal trials. J Nutr 137, 2513 S2523 S.
21. Velagapudi, VR, Hezaveh, R, Reigstad, CS, et al. (2010) The gut microbiota modulates host energy and lipid metabolism in mice. J Lipid Res 51, 11011112.
22. Peti-Peterdi, J, Kishore, BK & Pluznick, JL (2016) Regulation of vascular and renal function by metabolite receptors. Annu Rev Physiol 78, 391414.
23. Charles, JF, Ermann, J & Aliprantis, AO (2015) The intestinal microbiome and skeletal fitness: connecting bugs and bones. Clin Immunol 159, 163169.
24. Neuman, H, Debelius, JW, Knight, R, et al. (2015) Microbial endocrinology: the interplay between the microbiota and the endocrine system. FEMS Microbiol Rev 39, 509521.
25. Yano, JM, Yu, K & Donaldson, GP (2015) Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161, 264276.
26. Nicholson, JK, Holmes, E, Kinross, J, et al. (2012) Host-gut microbiota metabolic interactions. Science 336, 12621267.
27. Bäckhed, F, Ding, H, Wang, T, et al. (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101, 1571815723.
28. Bäckhed, F, Ley, RE, Sonnenburg, JL, et al. (2005) Host-bacterial mutualism in the human intestine. Science 307, 19151920.
29. Musso, G, Gambino, R, Cassader, M, et al. (2011) Interactions between gut microbiota and host metabolism predisposing to obesity and diabetes. Annu Rev Med 62, 361380.
30. Hooper, LV, Midtvedt, T & Gordon, JI (2002) How host–microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22, 283307.
31. Jumpertz, R, Le, DS, Turnbaugh, PJ, et al. (2011) Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am J Clin Nutr 94, 5865.
32. Vrieze, A, Van Nood, E, Holleman, F, et al. (2012) Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143, 913916.
33. Chevalier, C, Stojanović, O, Colin, DJ, et al. (2015) Gut microbiota orchestrates energy homeostasis during cold. Cell 163, 13601374.
34. Levenson, SM, Doft, F & Lev, M (1969) Influence of microorganisms on oxygen consumption, carbon dioxide production and colonic temperature of rats. J Nutr 97, 542552.
35. Levenson, SM (1978) The influence of the indigenous microflora on mammalian metabolism and nutrition. JPEN J Parenter Enteral Nutr 2, 78107.
36. Martin, DS (1932) The oxygen consumption of Escherichia coli during the lag and logarithmic phases of growth. J Gen Physiol 15, 691708.
37. Luong, JH & Volesky, B (1980) Determination of the heat of some aerobic fermentations. Can J Chem Eng 58, 497504.
38. Hoidal, JR, Beall, GD & Repine, JE (1979) Production of hydroxyl radical by human alveolar macrophages. Infect Immun 26, 10881092.
39. Rossouw, FM (1979) The effect of paraquat on the aerobic metabolism of rabbit alveolar macrophages and lung fibroblasts. S Afr Med J 55, 2023.
40. Racette, SB, Schoeller, DA, Luke, AH, et al. (1994) Relative dilution spaces of 2H-and 18O-labeled water in humans. Am J Physiol Endocrinol Metab 267, E585E590.
41. Bratteby, LE, Sandhagen, B, Fan, H, et al. (1997) A 7-day activity diary for assessment of daily energy expenditure validated by the doubly labelled water method in adolescents. Eur J Clin Nutr 51, 585591.
42. Fuller, Z, Horgan, G, O’Reilly, LM, et al. (2008) Comparing different measures of energy expenditure in human subjects resident in a metabolic facility. Eur J Clin Nutr 62, 560569.
43. Ndahimana, D & Kim, EK (2017) Measurement methods for physical activity and energy expenditure: a review. Clin Nutr Res 6, 6880.
44. Jequier, E, Acheson, K & Schutz, Y (1987) Assessment of energy expenditure and fuel utilization in man. Annu Rev Nutr 7, 187208.
45. Schoeller, DA (1988) Measurement of energy expenditure in free-living humans by using doubly labeled water. J Nutr 118, 12781289.
46. Tatner, P (1988) A model of the natural abundance of oxygen-18 and deuterium in the body water of animals. J Theor Biol 133, 267280.
47. Midwood, AJ, Haggarty, PA & McGaw, BA (1989) Methane production in ruminants: its effect on the doubly labeled water method. Am J Physiol Regul Integr Comp Physiol 257, R1488R1495.
48. Butler, PJ, Green, JA, Boyd, IL, et al. (2004) Measuring metabolic rate in the field: the pros and cons of the doubly labelled water and heart rate methods. Funct Ecol 18, 168183.
49. Midwood, AJ, Haggarty, PA & McGaw, BA (1993) The doubly labeled water method: errors due to deuterium exchange and sequestration in ruminants. Am J Physiol Regul Integr Comp Physiol 264, R561R567.
50. Bryant, JD & Froelich, PN (1995) A model of oxygen isotope fractionation in body water of large mammals. Geochim Cosmochim Acta 59, 45234537.
51. Gretebeck, RJ, Schoeller, DA, Socki, RA, et al. (1997) Adaptation of the doubly labeled water method for subjects consuming isotopically enriched water. J Appl Physiol 82, 563570.
52. Moritz, GL, Fourie, N, Yeakel, JD, et al. (2012) Baboons, water, and the ecology of oxygen stable isotopes in an arid hybrid zone. Physiol Biochem Zool 85, 421430.
53. Podlesak, DW, Torregrossa, AM, Ehleringer, JR, et al. (2008) Turnover of oxygen and hydrogen isotopes in the body water, CO2, hair, and enamel of a small mammal. Geochim Cosmochim Acta 72, 1935.
54. Berry, D, Mader, E, Lee, TK, et al. (2015) Tracking heavy water (D2O) incorporation for identifying and sorting active microbial cells. Proc Natl Acad Sci U S A 112, E194E203.
55. Levitt, MD (1971) Volume and composition of human intestinal gas determined by means of an intestinal washout technic. N Engl J Med 284, 13941398.
56. Carbonero, F, Benefiel, AC & Gaskins, HR (2012) Contributions of the microbial hydrogen economy to colonic homeostasis. Nat Rev Gastroenterol Hepatol 9, 504518.
57. Rotbart, A, Yao, CK, Ha, N, et al. (2017) Designing an in-vitro gas profiling system for human faecal samples. Sens Actuators B Chem 238, 754764.
58. Pitt, PA, De Bruijn, KM, Beeching, MF, et al. (1980) Studies on breath methane: the effect of ethnic origins and lactulose. Gut 21, 951954.
59. Bjørneklett, A & Jenssen, E (1982) Relationships between hydrogen (H2) and methane (CH4) production in man. Scand J Gastroenterol 17, 985992.
60. Livesey, G (1992) The energy values of dietary fibre and sugar alcohols for man. Nutr Res Rev 5, 6184.
61. Lifson, N & McClintock, R (1966) Theory of use of the turnover rates of body water for measuring energy and material balance. J Theor Biol 12, 4674.
62. Zhang, X, Gillespie, AL, Sessions, AL (2009) Large D/H variations in bacterial lipids reflect central metabolic pathways. Proc Natl Acad Sci U S A 106, 1258012586.
63. Kreuzer-Martin, HW, Lott, MJ & Dorigan, J (2003) Microbe forensics: oxygen and hydrogen stable isotope ratios in Bacillus subtilis cells and spores. Proc Natl Acad Sci U S A 100, 815819.
64. Vander Zanden, HB, Soto, DX, Bowen, GJ, et al. (2016) Expanding the isotopic toolbox: applications of hydrogen and oxygen stable isotope ratios to food web studies. Front Ecol Evol (epublication 16 March 2016).
65. Eve, IS (1966) A review of the physiology of the gastrointestinal tract in relation to radiation doses from radioactive materials. Health Phys 12, 131161.
66. Stephen, AM & Cummings, JH (1980) The microbial contribution to human fecal mass. J Med Microbiol 13, 4556.
67. Maskow, T & Paufler, S (2015) What does calorimetry and thermodynamics of living cells tell us? Methods 76, 310.
68. Cooney, CL, Wang, DI & Mateles, RI (1969) Measurement of heat evolution and correlation with oxygen consumption during microbial growth. Biotechnol Bioeng 11, 269281.
69. Russell, JB (1986) Heat production by ruminal bacteria in continuous culture and its relationship to maintenance energy. J Bacteriol 168, 694701.
70. Hackmann, TJ, Diese, LE & Firkins, JL (2013) Quantifying the responses of mixed rumen microbes to excess carbohydrate. Appl Environ Microbiol 79, 37863795.
71. Lepage, P, Leclerc, MC, Joossens, M, et al. (2012) A metagenomic insight into our gut’s microbiome. Gut 62, 146158.
72. Czerkawski, JW (1980) A novel estimate of the magnitude of heat produced in the rumen. Br J Nutr 43, 239243.
73. Liu, J-S, Marison, I & Von Stockar, U (1999) Anaerobic calorimetry of the growth of Lactobacillus helveticus using a highly sensitive Bio-RCl. J Therm Anal Calorim 3, 11911195.
74. Speakman, JR & Westerterp, KR (2010) Associations between energy demands, physical activity, and body composition in adult humans between 18 and 96 y of age. Am J Clin Nutr 92, 826834.
75. Conn, CA, Franklin, BR, Freter, RO, et al. (1991) Role of Gram-negative and Gram-positive gastrointestinal flora in temperature regulation of mice. Am J Physiol Regul Integr Comp Physiol 261, R1358R1363.
76. Kluger, MJ, Conn, CA, Franklin, BR, et al. (1990) Effect of gastrointestinal flora on body temperature of rats and mice. Am J Physiol Regul Integr Comp Physiol 258, R552R557.
77. Moore, WEC, Cato, EP & Holdeman, LV (1978) Some current concepts in intestinal bacteriology. Am J Clin Nutr 31, Suppl. 10, S33S42.
78. Espey, MG (2013) Role of oxygen gradients in shaping redox relationships between the human intestine and its microbiota. Free Radic Biol Med 55, 130140.
79. Cummings, JH (1981) Short chain fatty acids in the human colon. Gut 22, 763769.
80. McNeil, NI (1984) The contribution of the large intestine to energy supplies in man. Am J Clin Nutr 39, 338342.
81. Hershberger, TV & Hartsook, EW (1970) In vitro rumen fermentation of alfalfa hay. Carbon dioxide, methane, VFA and heat production. J Anim Sci 30, 257261.
82. Thomas, PC & Clapperton, JL (1972) Significance to the host of changes in fermentation activity. Proc Nutr Soc 31, 165170.
83. Webster, AJF (1978) Measurement and prediction of methane production, fermentation heat and metabolism in the tissues of the ruminant gut. In Ruminant Digestion and Feed Evaluation, pp. 8.18.10 [Osbourn, DF, Beever, DE and Thomson, DJ, editors]. London: Agricultural Research Council.
84. Bingham, S & Cummings, JH (1980) Sources and intakes of dietary fiber in man. In Medical Aspects of Dietary Fiber, pp. 261284 [Spiller, GA and McPherson Kay, R, editors]. Boston, MA: Springer.
85. Marston, HR (1948) The fermentation of cellulose in vitro by organisms from the rumen of sheep. Biochem J 42, 564574.
86. Russell, JB & Cook, GM (1995) Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev 59, 4862.
87. Westerhoff, HV, Hellingwerf, KJ & Van Dam, K (1983) Thermodynamic efficiency of microbial growth is low but optimal for maximal growth rate. Proc Natl Acad Sci U S A 80, 305309.
88. Meade, RD & Kenny, GP (2017) Are all heat loads created equal? Med Sci Sports Exerc 49, 17961804.
89. Blatteis, C, Boulant, J, Cabanac, M, et al. (2001) Glossary of terms for thermal physiology. Jpn J Physiol 51, 245280.
90. Schirmer, M, Smeekens, SP, Vlamakis, H, et al. (2016) Linking the human gut microbiome to inflammatory cytokine production capacity. Cell 167, 11251136.
91. Mifflin, MD, St Jeor, ST & Hill, LA (1990) A new predictive equation for resting energy expenditure in healthy individuals. Am J Clin Nutr 51, 241247.
92. Weijs, PJM (2008) Validity of predictive equations for resting energy expenditure in US and Dutch overweight and obese class I and II adults aged 18–65 y. Am J Clin Nutr 88, 959970.
93. McMurray, RG, Soares, J & Caspersen, CJ (2014) Examining variations of resting metabolic rate of adults: a public health perspective. Med Sci Sports Exerc 46, 13521358.
94. Henry, CJ (2005) Basal metabolic rate studies in humans: measurement and development of new equations. Public Health Nutr 8, 11331152.
95. Compher, C, Frankenfield, D, Keim, N, et al. (2006) Best practice methods to apply to measurement of resting metabolic rate in adults: a systematic review. J Am Diet Assoc 106, 881903.
96. Ou, JZ, Yao, CK, Rotbart, A, et al. (2015) Human intestinal gas measurement systems: in vitro fermentation and gas capsules. Trends Biotechnol 33, 208213.
97. Hylemon, PB, Harris, SC & Ridlon, JM (2018) Metabolism of hydrogen gases and bile acids in the gut microbiome. FEBS Lett 592, 20702082.
98. Konarzewski, M & Książek, A (2013) Determinants of intra-specific variation in basal metabolic rate. J Comp Physiol B 183, 2741.
99. Singh, V (1996) On-line measurement of oxygen uptake in cell culture using the dynamic method. Biotechnol Bioeng 52, 443448.
100. Wahlström, A, Sayin, SI, Marschall, HU, et al. (2016) Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism. Cell Metab 24, 4150.
101. Lefebvre, P, Cariou, B, Lien, F, et al. (2009) Role of bile acids and bile acid receptors in metabolic regulation. Physiol Rev 89, 147191.
102. Landsberg, L (2012) Core temperature: a forgotten variable in energy expenditure and obesity? Obes Rev 13, 97104.
103. Ockenga, J, Valentini, L, Schuetz, T, et al. (2012) Plasma bile acids are associated with energy expenditure and thyroid function in humans. J Clin Endocrinol Metab 97, 535542.
104. Klaassen, CD & Cui, JY (2015) Mechanisms of how the intestinal microbiota alters the effects of drugs and bile acids. Drug Metab Dispos 43, 15051521.
105. Vítek, L & Haluzík, M (2016) The role of bile acids in metabolic regulation. J Endocrinol 228, R85R96.
106. Long, SL, Gahan, CG & Joyce, SA (2017) Interactions between gut bacteria and bile in health and disease. Mol Aspects Med 56, 5465.
107. Institute of Medicine (2002) Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids. Washington, DC: The National Academies Press.
108. Pietinen, P, Rimm, EB, Korhonen, P, et al. (1996) Intake of dietary fiber and risk of coronary heart disease in a cohort of Finnish men. The Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study. Circulation 94, 27202727.
109. Rimm, EB, Ascherio, A, Giovannucci, E, et al. (1996) Vegetable, fruit, and cereal fiber intake and risk of coronary heart disease among men. JAMA 275, 447451.
110. Wolk, A, Manson, JE, Stampfer, MJ, et al. (1999) Long-term intake of dietary fiber and decreased risk of coronary heart disease among women. JAMA 281, 19982004.
111. Tungland, BC & Meyer, D (2002) Nondigestible oligo-and polysaccharides (dietary fiber): their physiology and role in human health and food. Compr Rev Food Sci Food Saf 1, 90109.
112. Behall, KM & Howe, JC (1995) Contribution of fiber and resistant starch to metabolizable energy. Am J Clin Nutr 62, 1158 S1160 S.
113. Livesey, G (1990) Energy values of unavailable carbohydrate and diets: an inquiry and analysis. Am J Clin Nutr 51, 617637.
114. Ashley, NT, Weil, ZM & Nelson, RJ (2012) Inflammation: mechanisms, costs, and natural variation. Annu Rev Ecol Evol Syst 43, 385406.
115. Bouchama, A & Knochel, JP (2002) Heat stroke. N Engl J Med 346, 19781988.
116. Lochmiller, RL & Deerenberg, C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 8798.
117. Roe, CF & Kinney, JM (1965) The caloric equivalent of fever II. Influence of major trauma. Ann Surg 161, 140147.
118. Muehlenbein, MP, Hirschtick, JL, Bonner, JZ, et al. (2010) Toward quantifying the usage costs of human immunity: altered metabolic rates and hormone levels during acute immune activation in men. Am J Hum Biol 22, 546556.
119. Walter, EJ, Hanna-Jumma, S, Carraretto, M, et al. (2016) The pathophysiological basis and consequences of fever. Crit Care 20, 200.
120. Westerterp, KR (2017) Control of energy expenditure in humans. Eur J Clin Nutr 71, 340344.
121. Verboeket-van de Venne, WPHG, Westerterp, KR, Hermans-Limpens, TJ, et al. (1996) Long-term effects of consumption of full-fat or reduced-fat products in healthy non-obese volunteers: assessment of energy expenditure and substrate oxidation. Metab Clin Exp 45, 10041010.
122. Westerterp, KR (2004) Diet induced thermogenesis. Nutr Metab (Lond) 1, 5.
123. Teixeira de Mattos, MJ & Tempest, DW (1983) Metabolic and energetic aspects of the growth of Klebsiella aerogenes NCTC 418 on glucose in anaerobic chemostat culture. Arch Microbiol 134, 8085.
124. Cook, GM & Russell, JB (1994) Energy-spilling reactions of Streptococcus bovis and resistance of its membrane to proton conductance. Appl Environ Microbiol 60, 19421948.
125. Steiner, AA (2017) The dynamic nature of resting metabolic rate. Temperature 4, 206207.
126. Wyman, JB, Heaton, KW, Manning, AP, et al. (1978) Variability of colonic function in healthy subjects. Gut 19, 146150.
127. Burg, TP, Godin, M, Knudsen, SM, et al. (2007) Weighing of biomolecules, single cells and single nanoparticles in fluid. Nature 446, 10661069.
128. Lewis, CL, Craig, CC & Senecal, AG (2014) Mass and density measurements of live and dead Gram negative and Gram positive bacteria populations. Appl Environ Microbiol 80, 36223631.
129. Macfarlane, S & Macfarlane, GT (2006) Composition and metabolic activities of bacterial biofilms colonizing food residues in the human gut. Appl Environ Microbiol 72, 62046211.
130. Sonnenburg, JL, Angenent, LT & Gordon, JI (2004) Getting a grip on things: how do communities of bacterial symbionts become established in our intestine? Nat Immunol 5, 569573.
131. Johansson, ME, Larsson, JMH & Hansson, GC (2011) The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci U S A 108, Suppl. 1, 46594665.
132. Hansson, GC (2012) Role of mucus layers in gut infection and inflammation. Curr Opin Microbiol 15, 5762.
133. Mowat, AM & Agace, WW (2014) Regional specialization within the intestinal immune system. Nature Rev Immunol 14, 667685.
134. Hartley, CL, Neumann, CS & Richmond, MH (1979) Adhesion of commensal bacteria to the large intestine wall in humans. Infect Immun 23, 128132.
135. Zoetendal, EG, von Wright, A, Vilpponen-Salmela, T, et al. (2002) Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl Environ Microbiol 68, 34013407.
136. Armstrong, LE, Lee, EC & Armstrong, EM (2018) Interactions of gut microbiota, endotoxemia, immune function, and diet in exertional heatstroke. J Sports Med (Hindawi Publ Corp) 2018, 5724575.
137. Magnúsdóttir, S, Heinken, A, Kutt, L, et al. (2017) Generation of genome-scale metabolic reconstructions for 773 members of the human gut microbiota. Nat Biotechnol 35, 8189.
138. Gordon, JI (2012) Honor thy gut symbionts redux. Science 336, 12511253.
139. Spor, A, Koren, O & Ley, R (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9, 279290.
140. Lozupone, CA, Stombaugh, JI, Gordon, JI, et al. (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489, 220230.
141. Atger, F, Mauvoisin, D, Weger, B, et al. (2017) Regulation of mammalian physiology by interconnected circadian and feeding rhythms. Front Endocrinol (Lausanne) 8, 42.
142. Burcelin, R (2012) Regulation of metabolism: a cross talk between gut microbiota and its human host. Physiol J 27, 300307.
143. Benson, AK, Kelly, SA, Legge, R, et al. (2010) Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci U S A 107, 1893318938.
144. Goodrich, JK, Waters, JL, Poole, AC, et al. (2014) Human genetics shape the gut microbiome. Cell 159, 789799.
145. Johnstone, AM, Murison, SD, Duncan, JS, et al. (2005) Factors influencing variation in basal metabolic rate include fat-free mass, fat mass, age, and circulating thyroxine but not sex, circulating leptin, or triiodothyronine. Am J Clin Nutr 82, 941948.
146. Xu, Z & Knight, R (2015) Dietary effects on human gut microbiome diversity. Br J Nutr 113, Suppl., S1S5.
147. David, LA, Maurice, CF, Carmody, RN, et al. (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559563.
148. Wu, GD, Chen, J, Hoffmann, C, et al. (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105108.
149. Falony, G, Joossens, M, Vieira-Silva, S, et al. (2016) Population-level analysis of gut microbiome variation. Science 352, 560564.
150. Barnett, JA (2003) Beginnings of microbiology and biochemistry: the contribution of yeast research. Microbiology 149, 557567.
151. Anukam, KC & Reid, G (2007) Probiotics: 100 years (1907–2007) after Elie Metchnikoff’s observation. In Communicating Current Research and Educational Topics and Trends in Applied Microbiology, pp. 466474 [Méndez-Vilas, A, editor]. Badajoz, Spain: Formatex Publishers.
152. Nelson, DP & Mata, LJ (1970) Bacterial flora associated with the human gastrointestinal mucosa. Gastroenterology 58, 5661.
153. Peach, S, Lock, MR, Katz, D, et al. (1978) Mucosal-associated bacterial flora of the intestine in patients with Crohn’s disease and in a control group. Gut 19, 10341042.
154. Croucher, SC, Houston, AP, Bayliss, CE, et al. (1983) Bacterial populations associated with different regions of the human colon wall. Appl Environ Microbiol 45, 10251033.
155. Langlands, SJ, Hopkins, MJ, Coleman, N, et al. (2004) Prebiotic carbohydrates modify the mucosa associated microflora of the human large bowel. Gut 53, 16101616.
156. Macfarlane, S, Furrie, E, Cummings, JH, et al. (2004) Chemotaxonomic analysis of bacterial populations colonizing the rectal mucosa in patients with ulcerative colitis. Clin Infect Dis 38, 16901699.
157. Havenith, G, Holmér, I & Parsons, K (2002) Personal factors in thermal comfort assessment: clothing properties and metabolic heat production. Energy Build 34, 581591.
158. Cramer, MN, Bain, AR & Jay, O (2012) Local sweating on the forehead, but not forearm, is influenced by aerobic fitness independently of heat balance requirements during exercise. Exp Physiol 97, 572582.
159. Gagnon, D, Jay, O & Kenny, GP (2013) The evaporative requirement for heat balance determines whole-body sweat rate during exercise under conditions permitting full evaporation. J Physiol 591, 29252935.
160. Hardy, JD & Stolwijk, JA (1966) Partitional calorimetric studies of man during exposures to thermal transients. J Appl Physiol 21, 17991806.
161. Stolwijk, JA & Hardy, JD (1966) Partitional calorimetric studies of responses of man to thermal transients. J Appl Physiol 21, 967977.
162. Adams, WC, Fox, RH, Fry, AJ, et al. (1975) Thermoregulation during marathon running in cool, moderate, and hot environments. J Appl Physiol 38, 10301037.



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