Definitions and Biochemical Pathways History (Literature Review) Use of Lipids to Build Proteins: Lab Mice & Polar Bears

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1 Definitions and Biochemical Pathways History (Literature Review) Use of Lipids to Build Proteins: Lab Mice & Polar Bears Use of Carbohydrates to Build Proteins: Tilapia Role of Gut Microbiome: Tilapia and Lab Mice Tracing Production from the Top Down: Kelp Forests Historical Ecology: Tracing Kelp Production Through Time

2 Amino Acids Non-Essential Ala, Gly, Ser, Asp, Glu, Pro, Arg, Tyr Essential Leu, Ileu, Phe, Thr, Val, Lys, Meth Lipids Fatty Acids Unsaturated: 16:1 / 18:1 / 18:2(n-6) / 20:4(n-6) / 20:5(n-3) Saturated: 14:0 / 16:0 / 18:0 Cholesterol Sugars, Starches, and Acids Sucrose / Glucose / Malate / Pyruvate

3 Essential Amino Acids Val Leu Ileu Phe Thr Routed from Dietary Protein (minimal isotopic alteration) Non-Essential Amino Acids Ala Gly Ser Glu Asp Arg Pro Carbon from Bulk Diet (carbohydrates & lipids & protein) Threonine Glycine

4 Non-Essential Alanine Glycine Serine Aspartic Acid Glutamic Acid Proline* Arginine* Hydroxyproline* Asparagine Cysteine* Glutamine* Selenocysteine* Tyrosine* Histidine* Ornithine* Taurine* *essential in some cases Essential Isoleucine Leucine Phenylalanine Threonine Valine Methionine Lysine Tryptophan

5 Food Amino Acid Pool Body Protein Glucose Pool Glycogen Neutral Fat Glycerol Fatty Acids 12 CO 2 3-Phosphoglycerate Pyruvate Glycolysis 12 C Gluconeogenesis Acetyl Group 12 Acetyl Group Acetyl CoA TCA Cycle 13 C 2 12 CO 2 Lipid Synthesis D 13 C: You Are What You Eat +0 2 Lipids have lower d 13 C values than muscle by 6 8

6 Glycine Serine Alanine Glucose 3-P-Glycerate Pyruvate Glycolysis (3) Essential AAs Leucine Isoleucine Phenyalanine Threonine Valine Acetyl - CoA Lipids Oxaloacetate Glutamine Aspartate TCA Cycle a-ketoglutarate Glutamate Arginine* Proline*

7 Non-Essential Essential 60-72% of amino acids in animal tissues are NON-ESSENTIAL

8 Phenylalanine Threonine Lysine Isoleucine Leucine Valine 30 40% Non-Essential Serine Glycine Tyrosine Aspartic Acid Glutamic Acid Proline Alanine 60 70%

9 La Padrina

10 ~20 Range in Amino Acid d 13 C in 1 Pig! Hare et al C 4 Pigs C 3 Pigs Similar patterns found in modern and fossil, terrestrial and marine, herbivores and carnivores

11 Glycine Serine Alanine Glucose 3-P-Glycerate Pyruvate Glycolysis (3) Essential AAs Leucine Isoleucine Phenyalanine Threonine Valine Acetyl - CoA Oxaloacetate Glutamine Aspartate TCA Cycle a-ketoglutarate Glutamate Arginine* Proline*

12 Non-Essentials Glutamic and Alanine Track Bulk Diet d 13 C Diet Contents: 20% Protein 70-80% Ground Corn/Wheat Essentials Leucine and Phenyalanine Track Dietary Amino Acid d 13 C Howland et al. 2003

13 Amphidon floridensis O Brien et al Adult diet (C 4 sugar) contributed 60% to non-essential AAs in hawkmoth eggs; essential amino acids sourced from larval (plant) diet

14 Definitions and Biochemical Pathways History (Literature Review) Examples: Use of Lipids to Build Proteins: Lab Mice & Polar Bears Use of Carbohydrates to Build Proteins: Tilapia Role of Gut Microbiome: Tilapia and Lab Mice Tracing Production from the Top Down: Kelp Forests Historical Ecology: Tracing Kelp Production Through Time

15 Lipids Lipids 6-8 d 13 C d 2 H Muscle Muscle + + Lipids adipose Protein muscle Amino/Fatty Acid Metabolism

16 D 13 Ctissue-protein Newsome et al. 2010

17 Newsome et al Glucose Protein (-27 ) Serine & Glycine D 13 C Pyruvate Alanine Oxaloacetate Acetyl CoA TCA Cycle a-ketoglutarate Glutamate (Arginine & Proline) Aspartate To what degree do animals use carbon from non-protein dietary sources (fat and carbs) to biosynthesize proteinaceous tissues?

18 Newsome et al Glucose Serine & Glycine D 13 C Pyruvate Alanine Oxaloacetate Acetyl CoA TCA Cycle Lipids (-15 ) a-ketoglutarate Glutamate (Arginine & Proline) Aspartate To what degree do animals use carbon from non-protein dietary sources (fat and carbs) to biosynthesize proteinaceous tissues?

19 Diet Treatments: C 3 Protein & C 4 Lipids/Sugar Newsome et al Weanling mice fed ad lib for 4 months (2 3x initial weight)

20 d 13 C Among Bulk Diets and Major Macromolecules Bulk Diets

21

22

23 C 4 Lipids Carbs C 3 Protein 40P:5F 30P:15F 20P:25F 5P:40F Newsome et al Diet Treatment Mice use lipid carbon to build non-essential amino acids, especially Glu and Asp.

24 40P:5F 30P:15F 20P:25F 5P:40F Newsome et al Diet Treatment Only dietary protein is used to synthesize mouse muscle essential amino acids

25 Amino Acid Pathway Casein Dietary Lipid Content 5% (6) 15% (7) 25% (7) 40% (6) Glycine (Gly) Glycolytic (0.8) (0.4) A (0.5) A (0.3) A (0.8) B Serine (Ser) Glycolytic (0.1) (0.7) A (0.8) A (0.7) A (1.1) B Alanine (Ala) Glycolytic (0.1) (0.3) A (0.7) A,B (0.7) B (1.3) B Aspartate (Asp) Krebs (0.1) (0.5) A (0.3) B (0.4) C (0.9) C Glutamate (Glu) Krebs (0.1) (1.0) A (0.2) B (0.7) C (1.6) B,C Proline (Pro) Krebs (0.1) (0.4) A (0.3) A (0.4) B (1.1) B TCA synthesized AAs: significant increases from 5% to 15% dietary lipid content. Glycolytic AAs: significant increases from 25% to 40% dietary lipid content.

26 Amino Acid Pathway Casein Dietary Lipid Content 5% (6) 15% (7) 25% (7) 40% (6) Glycine (Gly) Glycolytic (0.8) (0.4) A (0.5) A (0.3) A (0.8) B Serine (Ser) Glycolytic (0.1) (0.7) A (0.8) A (0.7) A (1.1) B Alanine (Ala) Glycolytic (0.1) (0.3) A (0.7) A,B (0.7) B (1.3) B Aspartate (Asp) Krebs (0.1) (0.5) A (0.3) B (0.4) C (0.9) C Glutamate (Glu) Krebs (0.1) (1.0) A (0.2) B (0.7) C (1.6) B,C Proline (Pro) Krebs (0.1) (0.4) A (0.3) A (0.4) B (1.1) B Leucine (Leu) Essential (0.1) (0.5) A (0.1) A (0.2) A (0.5) A Isoleucine (Ileu) Essential (0.4) (0.6) A (0.4) A (0.4) A (0.6) A Valine (Val) Essential (0.2) (0.6) A (0.5) A (0.6) A (1.2) A Phenylalanine (Phe) Essential (0.1) (0.5) A (0.3) A (1.0) A (0.5) A Bulk Muscle (0.7) A (0.3) A (0.6) B (0.4) C D 13 C Muscle-NLE (Bulk) Diet 1.7 (0.7) 0.5 (0.7) 0.2 (1.1) -1.1 (1.5) D 13 C Muscle-LE Diet 3.8 (0.7) 4.1 (0.4) 5.0 (0.6) 6.5 (0.4) Essential AAs: no significant differences among diet treatments.

27 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Hibernation Foraging/Breeding Summer Fast Foraging Hibernation DO NOT EAT EAT LITTLE DO NOT EAT Winter Fast Foraging/Breeding Summer Fast Foraging Winter Fast EAT LITTLE EAT LITTLE EAT LITTLE Polar Bears in the 21 st Century Face Two Challenges: #1: Abundance of preferred prey (ice seals) will likely decline. #2: Periods of fasting (especially summer) will likely increase.

28 Available Energy Exogenous Sources (seal protein and lipids) Digestion Assimilation Biosynthesis Anabolism Structural Tissues: Skeletal Muscle Adipose Tissue Energy Breath CO 2

29 Exogenous Sources (diet protein and lipids) Available Energy Digestion Assimilation Endogenous Sources Skeletal Muscle Adipose Tissue Energy Catabolism Mobilization Breath CO 2

30 Glycine Glucose Lipids ( 12 C) Serine Alanine Glucogenic AAs (non-essential) 3-P-Glycerate Pyruvate Acetyl CoA Glycolysis Lipids ( 12 C) Oxaloacetate Ketogenic AAs (non-essential) Glutamine Aspartate TCA Cycle a-ketoglutarate Glutamate Arginine* Proline* *75% of AAs in animal tissues

31 Exogenous Sources (diet protein and lipids) Available Energy VS Endogenous Sources (protein and lipid-rich tissues) Digestion Assimilation Accretion Mobilization Skeletal Muscle Red Blood Cells Adipose Tissue

32 Non-Essential Amino Acids Protein-Derived Carbon Glutamic Acid Lipid-Derived Carbon

33 Non-Essential Amino Acids Protein-Derived Carbon Glutamic Acid Lipid-Derived Carbon

34 Non-Essential Amino Acids Protein-Derived Carbon Glutamic Acid Lipid-Derived Carbon Protein-Derived Carbon Aspartic Acid Lipid-Derived Carbon

35 Non-Essential Amino Acids Protein-Derived Carbon Glutamic Acid Lipid-Derived Carbon Protein-Derived Carbon Aspartic Acid Lipid-Derived Carbon

36 Non-Essential Amino Acids Protein-Derived Carbon Glutamic Acid Lipid-Derived Carbon Protein-Derived Carbon Aspartic Acid Lipid-Derived Carbon Protein-Derived Carbon Alanine Lipid-Derived Carbon

37 Non-Essential Amino Acids Essential Amino Acids Glutamic Acid Phenylalanine Aspartic Acid Alanine

38 Non-Essential Amino Acids Essential Amino Acids Glutamic Acid Phenylalanine Aspartic Acid Isoleucine Alanine Leucine

39 Polar bears can use on-board fat stores (adipose) to maintain structural tissue during times of nutritional stress. Suggests an inherent amount of physiological plasticity Is it enough? Lipids adipose Protein muscle Non-Essential Amino Acid Metabolism

40 Definitions and Biochemical Pathways History (Literature Review) Examples: Use of Lipids to Build Proteins: Lab Mice & Polar Bears Use of Carbohydrates to Build Proteins: Tilapia Role of Gut Microbiome: Tilapia and Lab Mice Tracing Production from the Top Down: Kelp Forests Historical Ecology: Tracing Kelp Production Through Time

41 Wolf (~50kg) Consumes ~3 kg/day (Moose) Meat: ~15% Nitrogen 0.5 kg/day of N (~1% of body weight) Moose (~500kg) Consumes ~25 kg/day Vegetation: ~2% Nitrogen 0.5 kg/day N (~0.1% of body weight)

42 C 3 (-27 ) C 4 (-11 ) Nile Tilapia Oreochromis niloticus Kelly and Martinez del Rio 2010 To what degree does protein routing occur in an omnivorous ectotherm? Do mixing models, which assume that macromolecules are dissembled into elements and then reassembled into various compounds (e.g., amino acids), underestimate the contribution of dietary protein to overall diet? What proportion of the indispensable amino acid budget in tilapia is derived from gastrointestinal microbiota?

43 Complete Mixing Complete Routing Kelly and Martinez del Rio 2010 Suggests a large fraction of the carbon in indispensable amino acids in fish fed diets with <30% protein was derived from carbohydrates and lipids.

44 Glycolytic TCA Cycle Essentials

45 Glycine Glucose (C 4 Carbohydrates) Serine 3-P-Glycerate Alanine Pyruvate Acetyl CoA TCA Cycle

46 Glycolysis (Acetyl CoA) Aspartate Oxaloacetate TCA Cycle Arginine* Proline* a-ketoglutarate Glutamate

47

48 Applying amino acid specific discrimination factors from Larsen et al. (2009): Actinobacterium and Rhodococcus spp. grown on a sole-sucrose carbon source.

49 The incorporation of dietary protein carbon was dependent on dietary protein content and on each amino acids biosynthesis pathway. Glycolytic amino acids (Gly/Ser/Ala) reflected a large contribution of dietary carbohydrates and a small contribution of dietary protein. TCA cycle amino acids (Asp/Glu) paralleled bulk diet. Essential amino acids resembled that of carbohydrates at low protein intakes but were similar to their corresponding dietary amino acid as protein intake increased. This pattern is consistent with assimilation of microbially synthesized essential amino acids by tilapias fed low protein food. TAKE HOME: (1) Protein routing occurs in some dispensable amino acids and the scrambled egg assumption of mixing models is incorrect for omnivores. (2) CSIA is a novel method to quantify the contribution of symbiotic microbes to the indispensable amino acid budgets of animals.

50 Wolf (~50kg) Consumes ~3 kg/day Meat: ~15% Nitrogen 0.5 kg/day of N (~1% of body mass) Moose (~500kg) Consumes ~30 kg/day Vegetation: ~2% Nitrogen 0.5 kg/day N (~0.1% of body mass) Most animals live in a state of persistent or seasonal protein limitation.

51 What functional role do gut microbes play in contributing to observed plasticity in how wild animals utilize dietary macromolecules for metabolism and tissue synthesis?

52 39 Trillion Bacteria (~1 Pound)

53 Mammals have specialized organs (rumen and cecum) that host gut microbiota and interesting strategies (coprophagy) for dealing with low-quality resources. Percent Total Gut Volume Devoted to Fermentation White et al. 2012

54 While hexoses (glucose) and pentoses (xylose) are the most preferable soluble sugars for fermentation, they are bound in the structural components of plant cell walls (cellulose). The best way to stay firm and cute is by lowering Firmicutes White et al Number of Encoded Glycoside Hydrolases Glycoside hydrolases are the most common (intra- and extra-cellular) enzymes that assist in the hydrolysis of glycosidic bonds in complex sugars (e.g., cellulose).

55 10 14 Individuals >500 Species Illumina HiSeq NexGen Sequencer Thermo Delta V IRMS Eckburg et al These (technological) developments promise to deepen our understanding of human gut host-microbiota relationships and are readily applicable to other host-associated and free-living microbial communities. Dantas et al To trace the fate of non-protein dietary macromolecules used by the gut microbiome to synthesize amino acids that are shared with host organism to build structural tissues.

56 Nearly all work on the functional role of the mammalian gut microbiota has focused on carbohydrate metabolism since it dominates the modern human diet and is linked with disease. Average Animal or Bacteria Proteins Lipids Carbs Essential Amino Acids Val / Leu / Ileu / Phe / Thr Routed from Dietary Protein Threonine OR GUT MICROBIOTA? (carbohydrates & lipids)

57 Ingredient d 13 C ( ) Diet #1 (%) Diet #2 (%) Diet #3 (%) Diet #4 (%) Protein -26.5± Cornmeal -12.5± Sucrose -11.5± Cellulose -25.5± Lipids -11.5± Mice (10/treatment) fed diets for 4 months, culled, and tissues/guts collected Tissues: muscle, liver, blood plasma, red blood cells, hair Guts: duodenum, small intestine, ceca, large intestine

58 HIGH PROTEIN CONTENT LOW Firmicutes Firmicutes Bacteroidetes Bacteroidetes Diet #1 40C:40P Diet #2 45C:20P Diet #3 55C:10P Diet #4 75C:5P P = Protein % C = Carbohydrate % Higher Firmicutes:Bacteroidetes with decreasing dietary protein content.

59

60 Dietary Carbohydrates Amino acid specific fractionation factors for bacteria grown in culture on a single carbon source. (Larsen et al. 2009)

61

62

63 Abundance of Firmicutes:Bacteroidetes varied with dietary protein:carbohydrate content; also varied along intestinal tract (data not shown). As expected, the proportion of essential amino acids synthesized by gut microbiota and used by host to build structural tissues (muscle) varied with diet treatment: 5% (Phe) to 60% (Val) of tissue AA ESS budget in low protein diet. 0% (Thr) to 30% (Val) of tissue AA ESS budget in high protein diet. Preliminary modeling results jive with expectations based on biochemistry; e.g., valine is one of the simplest AA ESS to synthesize (via pyruvate). Firmicutes appear to be important in converting carbohydrates into essential amino acids that are used by the host to build structural tissues. Gut microbiota are likely an important component of their hosts protein metabolism, even for omnivorous animals that consume decent amounts of protein. LOTS TO DO! Physically separate bacteria phyla via flow cytometry and analyze amino acid d 13 C. Compare intestinal tissue with scat (non-invasive sampling of wild animals). Refine models

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