Proteins involved in fat-soluble vitamin and carotenoid transport across the intestinal cells: New insights from the past decade

It is now well established that vitamins D, E, and K and carotenoids are not absorbed solely through passive diffusion. Broad-specificity membrane transporters such as SR-BI (scavenger receptor class B type I), CD36 (CD36 molecule), NPC1L1 (Niemann Pick C1-like 1) or ABCA1 (ATP-binding cassette A1) are involved in the uptake of these micronutrients from the lumen to the enterocyte cytosol and in their secretion into the bloodstream. Recently, the existence of efflux pathways from the enterocyte back to the lumen or from the bloodstream to the lumen, involving ABCB1 (P-glycoprotein/MDR1) or the ABCG5/ABCG8 complex, has also been evidenced for vitamins D and K. Surprisingly, no membrane proteins have been involved in dietary vitamin A uptake so far. After an overview of the metabolism of fat-soluble vitamins and carotenoids along the gastrointestinal tract (from the mouth to the colon where interactions with microbiota may occur), a focus is placed on the identified and candidate proteins participating in the apical uptake, intracellular transport, basolateral secretion and efflux back to the lumen of fat-soluble vitamins and carotenoids in enterocytes. This review also highlights the mechanisms that remain to be identified to fully unravel the pathways involved in fat-soluble vitamin and carotenoid intestinal absorption.     

Proteins involved in uptake, intracellular transport and basolateral secretion of fat-soluble vitamins and carotenoids by mammalian enterocytes

Our understanding of the molecular mechanisms responsible for fat-soluble vitamin uptake and transport at the intestinal level has advanced considerably over the past decade. On one hand, it has long been considered that vitamin D and E as well as β-carotene (the main provitamin A carotenoid in human diet) were absorbed by a passive diffusion process, although this could not explain the broad inter-individual variability in the absorption efficiency of these molecules. On the other hand, it was assumed that preformed vitamin A (retinol) and vitamin K1 (phylloquinone) absorption occurred via energy-dependent processes, but the transporters involved have not yet been identified. The recent discovery of intestinal proteins able to facilitate vitamin E and carotenoid uptake and secretion by the enterocyte has spurred renewed interest in studying the fundamental mechanisms involved in the absorption of these micronutrients. The proteins identified so far are cholesterol transporters such as SR-BI (scavenger receptor class B type I), CD36 (cluster determinant 36), NPC1L1 (Niemann–Pick C1-like 1) or ABCA1 (ATP-Binding Cassette A1) displaying a broad substrate specificity, but it is likely that other membrane proteins are also involved. After overviewing the metabolism of fat-soluble vitamins and carotenoids in the human upper gastrointestinal lumen, we will focus on the putative or identified proteins participating in the intestinal uptake, intracellular transport and basolateral secretion of these fat-soluble vitamins and carotenoids, and outline the uncertainties that need to be explored in the future. Identifying the proteins involved in intestinal uptake and transport of fat-soluble vitamins and carotenoids across the enterocyte is of great importance, especially as some of them are already targets for the development of drugs able to slow cholesterol absorption. Indeed, these drugs may also interfere with lipid vitamin uptake. A better understanding of the molecular mechanisms involved in fat-soluble vitamin and carotenoid absorption is a priority to better optimize their bioavailability.     

Nutritional aspects of anastomotic operations with special reference to the sprue syndrome

Necessary but radical operation which results in short-circuits between various levels of the digestive tract, with or without resections of portions of the esophagus, stomach or intestine, frequently cures the condition for which the operation was done, but leaves the patient with difficult nutritional problems. These nutritional disturbances are usually associated with inability to maintain or gain weight as a result of badly regulated movement of food material through the altered digestive tract, and by the removal or diversion of important digestive secretions, such as those elaborated by the stomach, pancreas, duodenum and small bowel. Increased intestinal rate and diminished specific gastrointestinal secretions reduce the ability of the small bowel to properly absorb food, with resulting malnutrition, deficiency disease, and at times specific avitaminosis. Inability to absorb fat and fat-soluble substances is a constant feature of these conditions. Successful treatment of the nutritional problems involves constant, prolonged overfeeding of nonbulky foods, usually given in regular, frequently administered meals of small volume. Vitamin concentrates may occasionally be of some temporary assistance but are not needed if a balanced diet is given and may cause undesirable and sometimes dangerous symptoms. The use of supplemental substances, such as liver extract and a wetting agent, such as "Tween 80," to improve fat absorption have been demonstrated to be of value.The postoperative conditions described are fairly similar to the condition known as sprue, and it is possible that the general principles underlying the treatment of this disease apply to the entire group of post-operative nutritional disturbances alluded to.     

NUTRITIONAL ASPECTS OF ANASTOMOTIC OPERATIONS—With Special Reference to the Sprue Syndrome

Necessary but radical operation which results in short-circuits between various levels of the digestive tract, with or without resections of portions of the esophagus, stomach or intestine, frequently cures the condition for which the operation was done, but leaves the patient with difficult nutritional problems. These nutritional disturbances are usually associated with inability to maintain or gain weight as a result of badly regulated movement of food material through the altered digestive tract, and by the removal or diversion of important digestive secretions, such as those elaborated by the stomach, pancreas, duodenum and small bowel.Increased intestinal rate and diminished specific gastrointestinal secretions reduce the ability of the small bowel to properly absorb food, with resulting malnutrition, deficiency disease, and at times specific avitaminosis. Inability to absorb fat and fat-soluble substances is a constant feature of these conditions. Successful treatment of the nutritional problems involves constant, prolonged overfeeding of nonbulky foods, usually given in regular, frequently administered meals of small volume. Vitamin concentrates may occasionally be of some temporary assistance but are not needed if a balanced diet is given and may cause undesirable and sometimes dangerous symptoms. The use of supplemental substances, such as liver extract and a wetting agent, such as “Tween 80,” to improve fat absorption have been demonstrated to be of value.The postoperative conditions described are fairly similar to the condition known as sprue, and it is possible that the general principles underlying the treatment of this disease apply to the entire group of post-operative nutritional disturbances alluded to.     

Food factors and gastrointestinal function: a critical interface

The gastrointestinal tract (GIT) is an interface between the external environment and the body and functions to extract nutrients from foods as well as handle the various non-nutrient compounds found in foods. Thus factors in foods that affect health and disease may mediate their effects either through a direct effect on the GIT or indirectly by the pattern of absorption and subsequent metabolism through the GIT. To explore this relationship one must consider both the physiological responses of the GIT induced by factors in foods as well as the implications of GIT adaptation for metabolism. Metabolic adaptations to dietary factors such as cholesterol levels, glucose and insulin response, and immune function appear to be modulated by the manner in which food factors are metabolized in the GIT. New research is needed to understand the inter-relationship between food factors that stimulate GIT response and the subsequent influence on metabolism that influences risk factors for disease and health promotion.     

Quantification of fat-soluble vitamins in human breast milk by liquid chromatography-tandem mass spectrometry

Sensitive quantification method for fat-soluble vitamins in human breast milk by liquid chromatography-tandem mass spectrometry was developed. Vitamins A, D and E were extracted from 10.0 mL of breast milk after saponifying by basic condition. Vitamin K derivatives were extracted from 3.0 mL of breast milk after lipase treatment. The corresponding stable isotope-labeled compounds were used as internal standards. For the determination of vitamin D compounds, derivatization with a Cookson-type reagent was performed. All fat-soluble vitamins were determined by liquid chromatography-tandem mass spectrometry in the positive ion mode. The detection limits of all analytes were 1-250 pg per 50 microL. The recoveries of fat-soluble vitamins were 91-105%. Inter-assay CV values of each vitamin were 1.9-11.9%. The mean concentrations of retinol, vitamin D3, 25-hydroxyvitamin D3, alpha-tocopherol, phylloquinone and menaquinone-4 were 0.455 microg/mL, 0.088 ng/mL, 0.081 ng/mL, 5.087 microg/mL, 3.771 ng/mL, and 1.795 ng/mL, respectively (n=82). This method makes possible to determine fat-soluble vitamins with a wide range of polarities in human breast milk. The assay may be useful for large-scale studies.     

Physiology of intermittent feeding: integrating responses of vertebrates to nutritional deficit and excess

Food intakes of wild animals may not match their requirements for nutrients and energy but may vary between periods of nutritional excess (hyperphagia) and nutritional deficit (hypophagia) at timescales that vary from days to months. We present a simple model of feeding patterns and requirements of vertebrates. Frequent fasts and high intakes are typical of endothermic predators and migratory birds, whereas slow cycles and long deficits typify feeding patterns of ectothermic predators and ungulates in seasonal environments. We propose that hyperphagia is constrained by the ability to increase processes of digestion, absorption, intermediary metabolism, net deposition in tissue, and excretion to match loads of digesta and metabolites. Hyperphagia on high-quality diets is limited by the clearance of metabolites, whereas digestive tract capacity and flow limit consumption of low-quality diets. Of all digestive strategies, small omnivores with simple digestive systems may be the most tolerant of frequent hyperphagia. Tolerance of hypophagia favors large endogenous stores or low mass-specific rates of metabolism and reproductive output. Large animals may be most able to sustain reproduction during prolonged deficits in seasonal environments. Responses to excessive and deficient intakes of food are constrained by the length of the feeding cycle. Animals adapted to short feeding cycles may be best suited to unpredictable food supplies but at the energetic cost of maintaining spare capacity for digestion and absorption. Predictions of the response to food disruption are best evaluated in the context of body size, nutritional physiology, and life history of the species and the time for internal response.     

Nutraceuticals: facts and fiction

Epidemiological studies show a link between the consumption of plant-derived foods and a range of health benefits. These benefits have been associated, at least partially, to some of the phytochemical constituents, and, in particular, to polyphenols. In the last few years, nutraceuticals have appeared in the market. These are pharmaceutical forms (pills, powders, capsules, vials, etc.) containing food bioactive compounds as active principles. The bioactive phytochemicals have become a very significant source for nutraceutical ingredients. Scientific research supports the biological activity of many of these food phytochemicals, but the health claims attributed to the final marketed nutraceutical products have often little or doubtful scientific foundation. This is due to the fact that a lot of the scientific evidence is derived from animal testing and in vitro assays, whereas human clinical trials are scarce and inconclusive. Some key issues such as bioavailability, metabolism, dose/response and toxicity of these food bioactive compounds or the nutraceuticals themselves have not been well established yet. Amongst the phytochemicals, several groups of polyphenols (anthocyanins, proanthocyanidins, flavanones, isoflavones, resveratrol and ellagic acid) are currently used in the nutraceutical industry. In this report, we have reviewed the most recent scientific knowledge on the bioavailability and biological activity of these polyphenols ('fact'), as well as the health claims (which are not always supported by scientific studies) ascribed to the polyphenols-containing nutraceuticals ('fiction'). The in vitro antioxidant capacity, often used as a claim, can be irrelevant in terms of in vivo antioxidant effects. Bioavailability, metabolism, and tissue distribution of these polyphenols in humans are key factors that need to be clearly established in association to the biological effects of these polyphenols-containing nutraceuticals. The future trends of phytochemistry research regarding nutraceuticals are discussed.     

In vitro microbiotic fermentation causes an extensive metabolite turnover of rye bran phytochemicals

The human gut hosts a microbial community which actively contributes to the host metabolism and has thus remarkable effect on our health. Intestinal microbiota is known to interact remarkably with the dietary constituents entering the colon, causing major metabolic conversions prior to absorption. To investigate the effect of microbial metabolism on the phytochemical pool of rye bran, we applied an in vitro simulated colonic fermentation where samples were collected with intervals and analyzed by LC-MS based non-targeted metabolite profiling. The analyses revealed extensive metabolic turnover on the phytochemical composition of the bran samples, and showed effects on all the metabolite classes detected. Furthermore, the majority of the metabolites, both the precursors and the conversion products, remained unidentified indicating that there are numerous yet unknown phytochemicals, which can potentially affect on our health. This underlines the importance of comprehensive profiling assays and subsequent detailed molecular investigations in order to clarify the effect of microbiota on phytochemicals present in our everyday diet.     

Metabolism of dietary procyanidins in rats

Procyanidins are major dietary polyphenols made of elementary flavan-3-ol (epi)catechin units. They have antioxidant properties and may contribute to health benefits in humans, but little is known about their metabolic fate. We compared here the metabolism of procyanidin dimer B3, trimer C2, and polymer isolated from willow tree catkins to that of catechin monomer in rats. These compounds were administered in the rat diet (0.1%, w/w) for 5 d and their metabolites estimated in 24 h urine. In rats fed procyanidins, neither parent compound nor catechin derivatives could be detected in contrast to animals fed catechin monomer, which excreted large amounts of catechin and its 3'-O-methylated form (25.7 +/- 0.6%). On the other hand, 16 metabolites of microbial origin were detected and identified as phenylvaleric, phenylpropionic, phenylacetic, and benzoic acid derivatives. Their total yields significantly decreased from the catechin monomer (10.6 +/- 1.1%) to the procyanidin dimer (6.5 +/- 0.2%), trimer (0.7 +/- 0.1%), and polymer (0.5 +/- 0.1%). Therefore, the degree of procyanidin polymerization has a major impact on their fate in the body characterized by a poor absorption through the gut barrier and a limited metabolism by the intestinal microflora as compared to catechin. This will have to be considered to explain the health effects of procyanidins. The contribution of their microbial metabolites should also be further investigated.     

Vitamin Deficiencies in Humans: Can Plant Science Help?

The term vitamin describes a small group of organic compounds that are absolutely required in the human diet. Although for the most part, dependency criteria are met in developed countries through balanced diets, this is not the case for the five billion people in developing countries who depend predominantly on a single staple crop for survival. Thus, providing a more balanced vitamin intake from high-quality food remains one of the grandest challenges for global human nutrition in the coming decade(s). Here, we describe the known importance of vitamins in human health and current knowledge on their metabolism in plants. Deficits in developing countries are a combined consequence of a paucity of specific vitamins in major food staple crops, losses during crop processing, and/or overreliance on a single species as a primary food source. We discuss the role that plant science can play in addressing this problem and review successful engineering of vitamin pathways. We conclude that while considerable advances have been made in understanding vitamin metabolic pathways in plants, more cross-disciplinary approaches must be adopted to provide adequate levels of all vitamins in the major staple crops to eradicate vitamin deficiencies from the global population.     

Thematic Review Series: Bile Acids: Bile acids as regulatory molecules

In the past, bile acids were considered to be just detergent molecules derived from cholesterol in the liver. They were known to be important for the solubilization of cholesterol in the gallbladder and for stimulating the absorption of cholesterol, fat-soluble vitamins, and lipids from the intestines. However, during the last two decades, it has been discovered that bile acids are regulatory molecules. Bile acids have been discovered to activate specific nuclear receptors (farnesoid X receptor, preganane X receptor, and vitamin D receptor), G protein coupled receptor TGR5 (TGR5), and cell signaling pathways (c-jun N-terminal kinase 1/2, AKT, and ERK 1/2) in cells in the liver and gastrointestinal tract. Activation of nuclear receptors and cell signaling pathways alter the expression of numerous genes encoding enzyme/proteins involved in the regulation of bile acid, glucose, fatty acid, lipoprotein synthesis, metabolism, transport, and energy metabolism. They also play a role in the regulation of serum triglyceride levels in humans and rodents. Bile acids appear to function as nutrient signaling molecules primarily during the feed/fast cycle as there is a flux of these molecules returning from the intestines to the liver following a meal. In this review, we will summarize the current knowledge of how bile acids regulate hepatic lipid and glucose metabolism through the activation of specific nuclear receptors and cell signaling pathways.     

Basis for the historical stages for studying the biochemistry of vitamins. Noncoenzymatic mechanisms of vitamin B1

Biochemistry of vitamins is one of the leading trends in the fundamental researches of A. V. Palladin Institute of Biochemistry from the moment of its foundation in 1925. The Laboratory of Vitamins Biochemistry was organised in 1994, it was reorganized into the Department of Vitamins Biochemistry in 1966, and later it was renamed as the Department of Coenzymes Biochemistry. Now the investigations at the Coenzymes Biochemistry Department headed (from 1986) by G. V. Donchenko, Corr.-Member of the National Academy of Sciences of Ukraine, are directed to estimation of vitamins A, E, B1 and PP action molecular mechanisms. Investigation of specific protein-acceptors of vitamins and their biologically active derivatives is a contemporary and effective methodological approach to the estimation of some molecular mechanisms of vitamins action on cellular metabolism. Considering the challenging theoretical and practical aspects of the further fundamental investigation development in the molecular vitaminology the following items are currently being worked in the Department last time: 1. Study of some molecular mechanisms of thiamine and vitamin PP neurotropic action. These investigations are oriented to clearing some new aspects of noncoenzymic mechanism of its influence on the nervous cell functioning both in the norm and at some nervous diseases. 2. Study of some molecular mechanisms of regulation by means of fat-soluble vitamins A, E and their specific proteins-acceptors of DNA, RNA and protein biosynthesis in the nuclei and mitochondria of actively proliferous cells. These investigations are aimed to the estimation of molecular mechanisms of fat-soluble vitamins participation in the regulation of DNA-dependent synthesis of RNA, RNA-polymerase activity, mechanism of their anticancerogenous effect, vitamin E participation in the realisation of nuclear genetic information. 3. Study of intracellular protein-receptors, which take part in realisation of vitamins and their biologically active derivatives functions in the human and animals' organism. The investigations, directed to study of a role of retinol-binding proteins in exchange of the vitamin A and in biosynthesis of DNA, RNA and proteins, the role of tocopherol-binding proteins in realisation of biological action of vitamin E in cells and thiamine-binding proteins in realisation of neurotropic action of vitamin B1 are actively developed. 4. Investigation of mechanisms of antioxidizing and antiradical biological action of vitamin D3, ecdisterone and related biologically active compounds. Basing on the fundamental researches some vitamins preparations have been created, such as "Carotin-M", "Cardiovit", "Evit-1", "Soevit", "Metovit", "Caratel'ka" and others. The results of fundamental investigation of noncoenzymic thiamine function led us to elaboration of a new hypothesis about molecular mechanism of vitamin B1 neurotropic action. According to the hypothesis the thiamine high neuroactivity is a result of existence in the nervous ending a specific mobile thiamine pool and connection thiamine metabolism with nervous cell membrane potential and acetylcholine metabolism.     

Fatty acid alterations caused by PCBs (Aroclor 1242) and copper in adipose tissue around lymph nodes of mink

Fatty acid composition was determined in adipose tissue surrounding the mesenteric lymph nodes of mink (Mustela vison) exposed to polychlorinated biphenyls (PCBs: 1 mg Aroclor 1242 in food day⁻¹ for 28 days) and/or copper (62 mg kg⁻¹ food). These specific adipose tissues are known to have functional relationships with lymphocytes, and proliferation of cultured lymphocytes is influenced by the quality of fatty acids available in media. In six experimental groups the diet was based on freshwater fish, and in two groups it was based on marine fish. These basal diets differed in terms of fatty acid composition and content of fat-soluble vitamins A₁ and E. The fatty acid composition of membrane phospholipids (PL) responded to PCBs more than that of triacylglycerols (TG). The effects of copper were small. In female minks fed a diet of freshwater fish, the proportion of highly unsaturated fatty acids in PL decreased by 5 wt.% due to PCBs, and the acids seemed to be replaced by monounsaturated fatty acids (9 wt.% increase of total). This decrease of highly unsaturated fatty acids in PL was milder in minks on the marine fish diet rich in fat-soluble vitamins. In TG of minks on the marine diet, however, PCBs decreased the proportion of docosahexaenoic acid (22:6n-3). The possibility that these alterations in the fatty acid metabolism of adipose tissue supporting the lymph nodes affect immune function during PCB exposure should be studied further. Interestingly, the quality of the fish diet affected the magnitude of the alterations. The fatty acid responses may also differ between males and females.     

Vitamin K3 (menadione) and related quinones, like tumor-promoting phorbol esters, alter the affinity of epidermal growth factor for its membrane receptors

The effects of vitamin K3, quinones, fat-soluble vitamins, and various naturally occurring and synthetic compounds on the binding of 125I-epidermal growth factor (EGF) to mink lung cells or murine 3T3 cells in culture were studied. Vitamin K3, but not other fat-soluble vitamins, markeldy inhibits the binding of 125I-labeled EGF to treated cells, but does not affect the binding of insulin, concanavalin A, alpha-2-macroglobulin, and murine leukemia virus glycoprotein, gp70, to their membrane receptors. The binding of multiplication stimulating activity to treated cells is also reduced to some extent. Vitamin K3 alters the affinity of the receptors for EGF without changing the total number of available receptors per cell. Vitamin K3 modulation of EGF-receptor interaction is a temperature- and time-dependent phenomenon. EGF-receptor interaction is also significantly modulated by 1,4-naphthoquinone, 1,4-benzoquinone, and phenanthrenequinone but not by other quinones of anthracyclic antibiotics.     

Food deprivation induces differential changes in contents and microstructures of digestive tract and appendages in bluegill fish,Lepomis macrochirus

• 1.1. The digestive tract was compared with the tract appendages (caeca) in bluegill fish, Lepomis macrochirus in their response to short and long term food deprivation.
• 2.2. Fasting for 7 days resulted in 80% reduction of food content in the main tract, but only 40% reduction in appendages (caeca).
• 3.3. The intestine exhibited two different patterns of food distribution under fed and food deprived conditions.
• 4.4. The histopathological impact of starvation was more prominent on the intestine than on caeca.
• 5.5. These results suggest that digestive tract and appendages concommitantly conserve food during food scarcity, but appendages may offer advantages in retaining food longer, and in their greater resistance to starvation-induced effects.

     

Ultrastructure and histochemistry,of the stomach of Asplanchna sieboldi

Stomach cells of female Asplanchna sieboldi are specialized for absorption and intracellular digestion of nutrients. Evidence is presented to show that electron-opaque colloidal substances, present in the medium and within digestive vacuoles of the prey (Paramecium), are taken up by the stomach cells at the apical cell membrane and sequestered within food vacuoles which contain hydrolases working in both the acid and alkaline pH range. The stomach cells are also implicated in the absorption of molecules below the resolving power of the electron microscope. In rotifers possessing a complete digestive tract, this task is presumed to be handled by the intestine.     

Flavonoid antioxidants: chemistry,metabolism and structure-activity relationships

Flavonoids are a class of secondary plant phenolics with significant antioxidant and chelating properties. In the human diet, they are most concentrated in fruits, vegetables, wines, teas and cocoa. Their cardioprotective effects stem from the ability to inhibit lipid peroxidation, chelate redox-active metals, and attenuate other processes involving reactive oxygen species. Flavonoids occur in foods primarily as glycosides and polymers that are degraded to variable extents in the digestive tract. Although metabolism of these compounds remains elusive, enteric absorption occurs sufficiently to reduce plasma indices of oxidant status. The propensity of a flavonoid to inhibit free-radical mediated events is governed by its chemical structure. Since these compounds are based on the flavan nucleus, the number, positions, and types of substitutions influence radical scavenging and chelating activity. The diversity and multiple mechanisms of flavonoid action, together with the numerous methods of initiation, detection and measurement of oxidative processes in vitro and in vivo offer plausible explanations for existing discrepancies in structure-activity relationships. Despite some inconsistent lines of evidence, several structure-activity relationships are well established in vitro. Multiple hydroxyl groups confer upon the molecule substantial antioxidant, chelating and prooxidant activity. Methoxy groups introduce unfavorable steric effects and increase lipophilicity and membrane partitioning. A double bond and carbonyl function in the heterocycle or polymerization of the nuclear structure increases activity by affording a more stable flavonoid radical through conjugation and electron delocalization. Further investigation of the metabolism of these phytochemicals is justified to extend structure-activity relationships (SAR) to preventive and therapeutic nutritional strategies.     

黑水虻消化道形态及组织结构的观察

本文比较了不同发育阶段黑水虻Hermetia illucens消化道的形态学差异,掌握了幼虫消化系统的组织学特征。利用体视镜观察黑水虻5龄幼虫、预蛹及成虫的消化道形态,利用光学显微镜和扫描电镜观察幼虫消化道各段(前肠、中肠、后肠)的显微及超微结构。结果表明：黑水虻幼虫及预蛹的消化道均由前肠(食道和前胃)、中肠及后肠组成,从幼虫到成虫,消化道的长度不断缩短。与幼虫和预蛹相比,成虫消化道形态变化明显,前胃消失,出现了嗉囊及胃盲囊,中肠进一步缩短,后肠分化为回肠、结肠和直肠。组织学观察结果显示,幼虫的唾液腺开口于口腔,由膨大的管状腺体和腺管组成。食道由特化为角质刺突的内膜层及发达的肌层组成,其末端延伸至前胃。前胃膨大为球状,包括三层组织结构。根据上皮细胞形态的差异,中肠可分为四个区段。后肠薄,肠腔内褶丰富,肠壁可见数量较多的杆状细菌。马氏管开口于中、后肠交界处,包括4支盲管,管内壁密布微绒毛。黑水虻消化道形态随发育阶段的变化,反映了各阶段摄食及消化生理的差异。幼虫消化道各段具有各自典型的组织学特征,其前、中、后肠可能分别承担了食物接纳与初步消化、消化与吸收以及重吸收功能。本研究结果为进一步了...