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2 Using artificial diets to understand the nutritional
3 physiology of Drosophila melanogaster
4Q1 Matthew DW Piper
5 Artificial diets have been in use for rearing insects for more than that are concerned with breeding millions of individuals 42
6 100 years. Their composition ranges from completely for release in biological control. 43
7 chemically defined (holidic), to semi-defined (meridic) to non-
8 defined (oligidic). Recently, meridic and holidic diets have been
The development of diets for Drosophila 44
9 used to demonstrate previously unrecognised nutrient-
melanogaster 45
10 sensitive behaviours and patterns of fitness trait expression in
Drosophila melanogaster has a broad distribution that is
11 adult Drosophila melanogaster. This article presents a
largely dependent on its association with humans [3]. It 46
12 summary of the basic nutritional requirements of Drosophila
has been isolated from a variety of sources ranging from 47
13 followed by an account of some of these nutrient-modified
human excrement through to its more naturally assumed 48
14 phenotypes and what they can reveal about fundamental
abundance in rotting fruit [4]. Larval development and 49
15 mechanisms. Precisely controlled nutrition, combined with the
adult reproduction can occur rapidly in the latter envi- 50
16 many advantages of Drosophila present an ideal system for the
ronment where their diet is provisioned largely by 51
17 development of large scale metabolic modelling.
microbes involved in the process of decaying the fruit. 52
As a result, the nutritional requirements of Drosophila 53
Address
18Q2 School of Biological Sciences, Monash University, Clayton, Victoria closely match the biomass composition of microbes and 54
19 3800, Australia they have a healthy tolerance for the high alcohol content/ 55
low pH environments that accompany fermentative 56
Corresponding author: Piper, Matthew DW (matthew.piper@monash. metabolism [5]. On the basis of these parameters, flies 57
edu)
can readily be maintained in the laboratory on a diet of 58
sugar and yeast [6,7]. Despite this simplicity, a broad 59
20 Current Opinion in Insect Science 2017, 23:xx–yy range of lab diets have been developed that usually 60
21 This review comes from a themed issue on Molecular physiology incorporate some form of yeast as well as a variety of 61
24 2214-5745/ã 2017 Elsevier Inc. All rights reserved. dietary macronutrients can profoundly affect the expres- 67
sion of many phenotypes [9]. Thus, for the purposes of 68
standardisation and repeatability, several meridic [10–21] 69
and holidic [22,23] diets have been developed for 70
Drosophila. The components of these diets are sum-
marised in Table 1. Q371
25 Introduction
26 The practice of rearing insects on artificial diets can be The greatest challenge that faces researchers looking to 72
27 traced back to at least 1908 when the blue bottle fly develop synthetic diets is complexity. Organisms require 73
28 (Calliphora vomitoria) was reared from egg to adult on a several dozen nutrients to grow, reproduce and survive 74
29 diet of meat extract, starch, peptone and mineral salts and the degree to which each is required varies with the 75
30 [1,2]. As the range of insects reared in the laboratory has organisms genotype, age and environment. Thus, a die- 76
31 broadened, so too have the research questions, which has tary formulation that is optimal for female egg laying 77
32 introduced the demand for different levels of control over under laboratory conditions, may not be optimal to sup- 78
33 nutrition. Diets can range in nutritional precisions from port development. While this complexity can be frustrat- 79
34 completely chemically defined (holidic), to diets made of ing and overwhelming, it is also the essential feature of 80
35 a mixture of chemically defined components and one or synthetic diets: they provide a format for generating 81
36 two non-defined ingredients (meridic) to diets made nutrient omissions and/or imbalances that can reveal 82
37 completely from crude organic materials (oligidic; defini- mechanistic information about organismal physiology. 83
38 tions from [2]). These service the requirements of exper- Here, I provide a summary of what we know to be the 84
39 imental biologists engaged in activities ranging from nutritional requirements of Drosophila melanogaster, and in 85
40 attempts to understand the precise details of nutritional doing so, highlight both gaps in our knowledge as well as 86
41 physiology, through to large scale rearing programmes examples of how precise manipulations of individual 87
Please cite this article in press as: Piper MDW: Using artificial diets to understand the nutritional physiology of Drosophila melanogaster, Curr Opin Insect Sci (2017), http://dx.doi.org/10.1016/j.
cois.2017.07.014
Current Opinion in Insect Science 2017, 23:1–8
2 Molecular physiology
Reference a Villee and Hinton et al. Hinton Sang et al. Sang and Geer Geer van Rapport ReisTroen et al. Lee and Piper et al. Piper et al. Lange and
Bissell (1951) (1956) (1956) King (1963) and Herrewege et al. (2016) (2007, Michelli (2014)b (2017) Heijnen
(1948) (1961) Vovis (1974) (1984) 2010 (2013) (2001)
(1965) erratum)
Details Table IV Medium 4; Table II Medium C; Medium D Figure 2 Table 10 Table 4 Table 2 Table 1 Harlan CDF400K; 50S200N 50S 200N Reconciled
Tables 1 Table 11 Teklad suppl. HUNTaa; FLYaa; biomass of
and 20 TD.04310; tables Figures 1 Figures 5 yeast;
Table 2 and 5 and 7 Table VIIIc
Minimum dev 8.2/11.4 7.5/N.A. e 10.4/N.A. 4.8/9.1 f N.A. 6.4g/N.A. 12.3/N.A. N.A. 8.7/N.A. N.A./10.36 N.A. 8.85/13.23 9.9/N.A. N.A./14.7
time (d) d
Dev on yeast 4/N.A. 5.4/N.A. N.A. 3.9/8.2 N.A. N.A. N.A. N.A. 6.1/N.A. N.A. N.A. 4.71/8.61 4.9/N.A. N.A.
control
Adult egg laying N.A. N.A. N.A. N.A. Ave 69% of N.A. N.A. N.A. N.A. N.A. N.A. Max 366% of Ave 80% 100% of
yeast food yeast food h of yeast yeast food
food
Adult lifespan N.A. N.A. N.A. N.A. N.A. N.A. N.A. 52.7 N.A. 63 f i 75 f 37 f/43 m j 61 f 8 72 f 8
f/42.6 m
g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l %k
Agar 15 15 20 30 15 15 15 10 5 20 10 20 20
Carbohydrate 38.7
Glucose 150 5.93
Fructose 7.5 10
Sucrose 50 7.5 7.5 7.5 10 7.5 10 13.3 63.68 17.12 17.12
Lactose 4.92
Trehalose 3.91
Casein 20 55 55 50 10 73.3 40.7 l
L-alanine 1.09 3.3 0.5 0.26 1.11 2.12 1.1
L-arginine 0.80 0.5m 3.025 0.8 0.8 0.39 1.67 0.48 1.63
L-asparagine 0.25 0.53 1.03 1.03
L-aspartate 1.22 3.3 0.5 0.53 1.03 1.17
L-cysteine 0.4 0.48 0.48 1.1 0.3 0.5 0.10 0.43 0.061 0.34
L-glutamate 4.42 4.42 8.53 8.4 5.4 0.56 1.2 1.51 1.52
L-glutamine 1.2 1.51 1.12
Glycine 1.75 1.75 1.65 0.4 0.5 0.10 0.43 1.94 0.77
L-histidine 0.48 0.48 1.65 1 1 0.11 0.47 0.61 0.65
L-isoleucine 1.26 1.26 3.85 3 3 0.19 0.81 1.82 1.12
L-leucine 2.35 2.35 4.68 2 2 0.31 1.32 1.21 2.03
L-lysine 1.34 1.34 4.4 1.9 0.65 2.78 1.15 1.37
L-methionine 0.34 0.34 1.65 0.8 0.8 1.35 0.58 0.48 0.6
L-phenylalanine 1.008 1.008 3.03 1.3 1.3 0.22 0.94 0.79 1.01
L-proline 1.68 4.4 0.5 0.21 0.9 0.91 0.98
L-hydroxyproline 0.38
www.sciencedirect.com
Reference a Villee and Hinton et al. Hinton Sang et al. Sang and Geer Geer van Rapport Reis Troen et al. Lee and Piper et al. Piper et al. Lange and
Bissell (1951) (1956) (1956) King (1963) and Herrewege et al. (2016) (2007, Michelli (2014)b (2017) Heijnen
(1948) (1961) Vovis (1974) (1984) 2010 (2013) (2001)
(1965) erratum)
Details Table IV Medium 4; Table II Medium C; Medium D Figure 2 Table 10 Table 4 Table 2 Table 1 Harlan CDF400K; 50S200N 50S 200N Reconciled
Tables 1 Table 11 Teklad suppl. HUNTaa; FLYaa; biomass of
and 20 TD.04310; tables Figures 1 Figures 5 yeast;
Table 2 and 5 and 7 Table VIIIc
Minimum dev 8.2/11.4 7.5/N.A. e 10.4/N.A. 4.8/9.1 f N.A. 6.4g/N.A. 12.3/N.A. N.A. 8.7/N.A. N.A./10.36 N.A. 8.85/13.23 9.9/N.A. N.A./14.7
time (d) d
Dev on yeast 4/N.A. 5.4/N.A. N.A. 3.9/8.2 N.A. N.A. N.A. N.A. 6.1/N.A. N.A. N.A. 4.71/8.61 4.9/N.A. N.A.
control
Adult egg laying N.A. N.A. N.A. N.A. Ave 69% of N.A. N.A. N.A. N.A. N.A. N.A. Max 366% of Ave 80% 100% of
yeast food yeast food h of yeast yeast food
food
Adult lifespan N.A. N.A. N.A. N.A. N.A. N.A. N.A. 52.7 N.A. 63 f i 75 f 37 f/43 m j 61 f 8 72 f 8
f/42.6 m
g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l %k
Ergosterol 1
Inositol 0.042 0.042 0.042 0.005 0.005
Choline 0.02 0.02 0.075 0.04 0.08 0.06 0.06 0.32 0.016 0.036 0.05 0.05
RNA 1 1 4 4 1 4 1 1 6.6
DNA 0.5 0.3
Adenine 0.2–1.0 0.3 0.6o
Guanine 0.25 0.4
Cytosine 0.2 0.4
Uracil 0.18 0.4
Thymidine 0.004 0.2
Inosine 0.25 0.85 0.065 0.065
Uridine 0.76 0.06 0.06
Metals p 2.5 q
Calcium 0.0065 0.013 0.013 0.0129 0.05 0.0046 0.013 0.25 0.25
Chloride 0.013 0.039 0.039 0.13 0.0258 0.016 0.301 0.301
Chromium 0.00056 0.0054
Current Opinion in Insect Science 2017, 23:1–8
4 Molecular physiology
Table 1 (Continued )
Reference a Villee and Hinton et al. Hinton Sang et al. Sang and Geer Geer van Rapport Reis Troen et al. Lee and Piper et al. Piper et al. Lange and
Bissell (1951) (1956) (1956) King (1963) and Herrewege et al. (2016) (2007, Michelli (2014)b (2017) Heijnen
(1948) (1961) Vovis (1974) (1984) 2010 (2013) (2001)
(1965) erratum)
Details Table IV Medium 4; Table II Medium C; Medium D Figure 2 Table 10 Table 4 Table 2 Table 1 Harlan CDF400K; 50S200N 50S 200N Reconciled
Tables 1 Table 11 Teklad suppl. HUNTaa; FLYaa; biomass of
and 20 TD.04310; tables Figures 1 Figures 5 yeast;
Table 2 and 5 and 7 Table VIIIc
Minimum dev 8.2/11.4 7.5/N.A. e 10.4/N.A. 4.8/9.1 f N.A. 6.4g/N.A. 12.3/N.A. N.A. 8.7/N.A. N.A./10.36 N.A. 8.85/13.23 9.9/N.A. N.A./14.7
time (d) d
Dev on yeast 4/N.A. 5.4/N.A. N.A. 3.9/8.2 N.A. N.A. N.A. N.A. 6.1/N.A. N.A. N.A. 4.71/8.61 4.9/N.A. N.A.
control
Adult egg laying N.A. N.A. N.A. N.A. Ave 69% of N.A. N.A. N.A. N.A. N.A. N.A. Max 366% of Ave 80% 100% of
yeast food yeast food h of yeast yeast food
food
Adult lifespan N.A. N.A. N.A. N.A. N.A. N.A. N.A. 52.7 N.A. 63 f i 75 f 37 f/43 m j 61 f 8 72 f 8
f/42.6 m
g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l g/l %k
vitA 1350 IU 1350 IU
vitE 16.5 IU 16.5 IU
vitD 335 IU 335 IU
vitK 0.0005 0.00051
a
Several references not included due to ambiguity about the concentration of the components and/or repetition of similar diets between different studies (e.g. several using Sangs Medium C).
b
Detailed account of the latest diet preparation protocol can be found at www.piperlab.org/resources or https://doi.org/10.1371/journal.pbio.2000862.
c
Statistically reconciled biomass composition of dried S. cerevisiae during steady-state cultivation in a carbon-limited chemostat, growing at a dilution rate of 0.1 hour 1.
d
Data are presented as days from ‘egg to pupa/egg to adult’, where available.
e
Information not available (N.A.).
f
4.3d was added for pupariation according to authors’ estimate.
g
Best for CantonS.
h
Lifetime reproduction for CDF300K versus regular food.
i
Median lifespan for females (f).
j
Median lifespan.
k
Approximates g/l for our standard sugar/yeast food, which contains 100 g/l dried S. cerevisiae.
l
Yeast protein.
m
Optimum from a range of concentrations.
n
As 60% fat, 40% phospholipids; acyl groups as 44 palmitoleic: 17 oleic: 14 palmitic: 10 stearic acids; phospholipid substitutions as 23 ethanolamine: 62 choline: 16 serine.
www.sciencedirect.com
o
Bases added in monophosphate form.
p
Na and K are present in all diets, but not itemised due to contributions as salts from other components and/or pH control.
q
On the basis of measured Ca, Cu, Fe, K, Mg, Mn, Na, Zn.
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COIS 390 1–8
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308 nutrients have revealed insights into the determinants of and unpublished data). However, the delay can be 370
317 physiological states. reduced to 25% with the addition of a small amount 371
of water-soluble yeast extract [23]. A similarly small 372
318 Basic nutritional requirements developmental delay was reported by Sang for his 373
319 As opposed to microbes that can assimilate much of Medium C, a meridic medium that contained the non- 374
320 their biomass from elements, higher organisms generally purified components casein, lecithin and yeast ribonu- 375
321 require a supply of macromolecules to drive metabolic cleic acid [13,15]. Given the positive relationship 376
322 physiology. For Drosophila, an adequate mixture of nutri- between growth rate and the content of nitrogen, phos- 377
323 ents contains carbohydrates (source of carbon and phorous, RNA and DNA in the developing larva [28] it is 378
324 energy), amino acids (source of nitrogen, carbon, energy reasonable to suspect that the yeast RNA in Sangs 379
325 and sulfur), a sterol (cholesterol or ergosterol), choline, medium overcame a nucleic acid and/or phosphorous 380
326 inosine, uridine, myo-inositol, as well as a mixture of limitation in holidic media. However, addition of all 381
327 B-group vitamins (B1/thiamine, B2/riboflavin, B3/nico- nucleosides or nucleoside triphosphates cannot rectify 382
328 tinic acid, B5/pantothenate, B6/pyridoxine, B7/biotin, the delay ([22,23] and unpublished data). Another, 383
329 B9/folic acid) and trace elements including metal ions unexplored, but testable alternative is that intake and 384
330 (potassium, sodium, phosphorous, chlorine, calcium, digestion of casein and yeast proteins provides peptides or 385
331 copper, iron, magnesium, manganese and zinc) ([23] other metabolites that act as ligands to stimulate signal- 386
332 and unpublished observations). Although other insects ling pathways that are important for growth, similar to the 387
333 exhibit a requirement for essential fatty acids, and bioactive components found in human milk [29]. Finally, 388
Drosophila lacks the relevant desaturases for de novo it is also possible that the deficiency is non-nutritious, 389
334 synthesis [24], evidence from radiolabelled tracer and reflecting some physical property of the medium and/or a 390
335 rearing studies show Drosophila do not require any fatty complex odour or tastant to make it attractive. Our initial 391
336 acids in their diets [22,23,25]. Further additions of anti- attempts to address this by adding insoluble cellulose for 392
337 biotics, short-chain acids and methylparaben (nipagin/ texture or phenylethanol to enhance the mediums attrac- 393
338 food preservative E218) to act as antimicrobial preserva- tiveness [30] were unsuccessful (unpublished observa- 394
339 tives are also often made. In this context it is worth noting tions). Given these uncertainties, researchers who seek to 395
340 that short chain acids such as propionic acid can also act as control developmental nutrition but who want to avoid 396
341 a source of energy for flies. It can be observed that the substantial delays found when using holidic diets, 397
342 molybdenum is not listed above, and it is not in any may find meridic diets to be a useful intermediate. 398
343 defined medium published to date (Table 1). However, it
344 could be important for longer term health as it is thought Adult 399
345 to affect purine metabolism for uric acid production, There are a few reports addressing the nutritional require- 400
346 which is important for nitrogen excretion in flies [26] ments of adult Drosophila, and the basic constituents of an 401
Please cite this article in press as: Piper MDW: Using artificial diets to understand the nutritional physiology of Drosophila melanogaster, Curr Opin Insect Sci (2017), http://dx.doi.org/10.1016/j.
cois.2017.07.014
COIS 390 1–8
6 Molecular physiology
425 sterols, sugar, amino acids (all or any one essential amino egg laying [39]. Notably, although the amino acid ratio 481
426 acid), vitamins or metal ions causes reduced egg laying as modified egg production, lifespan was insensitive to the 482
427 well as reduced lifespan [15,23]. However, the severity ratio — responding only to the total mass of dietary amino 483
428 of each deficiency on these traits is not equal, demon- acids. Thus, the degree to which dietary amino acids were 484
429 strating the varying value of different nutrients to fulfil incorporated into eggs was not relevant for lifespan, 485
430 different physiological outcomes. For example, omitting meaning that excretory load, and thus dietary protein 486
431 the majority of metal ions (but not K, Ca or Mg) quickly toxicity, is less likely to account for the effects of amino 487
432 stopped egg laying, but had no effect on lifespan, whereas acids on lifespan than high TOR signalling causing 488
433 removing the sterol source (cholesterol) had only a rela- reduced proteostasis. Future studies to understand the 489
434 tively minor effect on egg laying, but caused dramatic details of how amino acids are used by the body will be 490
435 lifespan shortening [23]. This can be explained if the informative to understand the mechanistic bases of repro- 491
436 checkpoints for egg development are sensitive to the duction and longevity assurance. 492
437 absence of diet derived metal ions, but not sterols. Thus
438 when there is no renewable source of metal ions, invest- Behaviour 493
439 ment into eggs is halted and the adult fly is preserved. Holidic diets have been used to study how nutritional 494
440 However, when dietary sterols are lacking, investment of components modulate activity. In particular, both the 495
441 adult derived sterols into eggs may be used to preserve perceived and nutritional values of low versus high die- 496
442 egg viability [15], but severely cost the mother in terms of tary sugar modulate sleep partitioning in flies by changing 497
443 survival. Thus, precise nutritional interventions can pro- the flies’ arousal threshold [40]. This is speculated to be 498
444 vide information to inform mechanistic studies. part of an adaptive response whereby flies are more likely 499
to stay close to a rich source of energy rather than 500
445 Less severe diet manipulations can also be highly infor- undertaking a costly foraging trip. The decision-making 501
446 mative about the mechanisms that regulate nutritional about foraging can also be affected by amino acid status. 502
447 physiology. Mild dietary restriction increases lifespan and Recent work has shown that the flies’ dietary amino acid 503
448 decreases reproduction, a relationship that has tradition- histories interact with mating status to affect their ten- 504
449 ally been attributed to the way dietary energy is utilised dency to initiate, continue and stop feeding as well as the 505
450 [33,34]. More recently, it has been recognised that the range they explore while foraging [41]. Notably, these 506
451 same inverse relationship between lifespan and reproduc- behavioural changes were specific to proteinaceous food, 507
452 tion can be elicited by lowering the dietary protein: and did not affect feeding behaviour around sucrose 508
453 carbohydrate ratio while caloric intake is held constant patches. In additional detailed work using holidic media, 509
454 [35,36]. These experiments were initially performed it was shown that protein-specific appetite could be 510
455 with oligidic diets, but the findings have been more stimulated by removing any one of the 10 essential amino 511
456 recently reproduced using meridic and holidic media in acids from the diet, but not by removing any of the 512
457 which yeast-derived protein is replaced by an amino acid 10 non-essentials. Interestingly, flies that were geneti- 513
458 mixture [23,37,38]. Two, potentially competing, mecha- cally altered to lack the ability to synthesise the non- 514
459 nistic explanations have been put forward for why life- essential amino acid tyrosine, could acquire a protein 515
460 span is decreased by a high protein: carbohydrate ratio. appetite in response to tyrosine deficient food. This 516
461 The first is that chronic consumption of a relatively high demonstrated that signalling to trigger protein appetite 517
462 protein diet constitutively activates TOR signalling, is not specifically tuned to the 10 essential amino acids 518
463 which reduces quality control over the proteome by but can also be elicited when a non-essential amino acid 519
464 suppressing protein turnover (lowered proteostasis). becomes limiting [42]. Curiously, amino acid motivated 520
465 Alternatively, high protein diets exert chronic excretory feeding was also modulated by signals from the flies’ 521
466 costs that become critical as ageing-related systems microbiome possibly via an independent mechanism 522
467 decline (protein toxicity). One test to distinguish [42]. Thus holidic diets have begun to expose different 523
468 between these possibilities is to assess the independent molecular interactions that flies employ to redress fine- 524
469 effects of protein quality and quantity since high quality scale nutritional imbalances. Establishing this ground- 525
470 protein should continue to activate TOR, but reduce the work serves as an invaluable vantage point from which 526
471 costs of excretion due to greater utilisation efficiency (e.g. to begin disentangling the underlying neuronal signalling 527
472 for egg laying). However, such a test requires a definition and circuitry that drive these decisions. 528
473 of protein quality — an intractable problem to solve
474 empirically given that the nutrient space to explore con- Defined media as a platform for modelling complex 529
475 sists of 20 amino acid dimensions. We recently described metabolic interactions 530
476 a method we termed exome matching that models the Understanding the details of nutrient uptake and absorp- 531
477 dietary amino acid ratio on the in silico translated exome tion and how these relate to biomass production and 532
478 of the consumer. Using our holidic medium, we demon- metabolic rates is the starting point for establishing nutri- 533
479 strated that exome matching produces a theoretical defi- ent budgets. In combination with knowledge of the 534
480 nition of high quality protein equivalents for growth and organisms metabolic biochemistry, these budgets can 535
Please cite this article in press as: Piper MDW: Using artificial diets to understand the nutritional physiology of Drosophila melanogaster, Curr Opin Insect Sci (2017), http://dx.doi.org/10.1016/j.
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674 high protein: low carbohydrate: high fat diets yield the shortest lifespans. large-scale metabolic models to identify novel markers for personalised 719
675 This study additionally serves as the basis of a series of articles describing medicine in humans. 720
676 other physiological parameters of these mice.
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Please cite this article in press as: Piper MDW: Using artificial diets to understand the nutritional physiology of Drosophila melanogaster, Curr Opin Insect Sci (2017), http://dx.doi.org/10.1016/j.
cois.2017.07.014