Vital Staining of the Stick Insect Digestive System Identifies Appendices of the Midgut as Novel System of Excretion (original) (raw)
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Arthropod Structure & Development, 2014
This work presents a detailed morphofunctional study of the digestive system of a phasmid representative, Cladomorphus phyllinus. Cells from anterior midgut exhibit a merocrine secretion, whereas posterior midgut cells show a microapocrine secretion. A complex system of midgut tubules is observed in the posterior midgut which is probably related to the luminal alkalization of this region. Amaranth dye injection into the haemolymph and orally feeding insects with dye indicated that the anterior midgut is water-absorbing, whereas the Malpighian tubules are the main site of water secretion. Thus, a putative counter-current flux of fluid from posterior to anterior midgut may propel enzyme digestive recycling, confirmed by the low rate of enzyme excretion. The foregut and anterior midgut present an acidic pH (5.3 and 5.6, respectively), whereas the posterior midgut is highly alkaline (9.1) which may be related to the digestion of hemicelluloses. Most amylase, trypsin and chymotrypsin activities occur in the foregut and anterior midgut. Maltase is found along the midgut associated with the microvillar glycocalix, while aminopeptidase occurs in the middle and posterior midgut in membrane bound forms. Both amylase and trypsin are secreted mainly by the anterior midgut through an exocytic process as revealed by immunocytochemical data.
PLOS ONE
The Malpighian tubules are the insect excretory organs, responsible for ion and water homeostasis and elimination of nitrogenous wastes. Post-genomic assays suggest they also metabolize and detoxify xenobiotic compounds and have antimicrobial properties. The Phasmatodea have an additional, unique set of excretory organs referred to predominantly as midgut appendices. Their function and how it compares to phasmid and other insect Malpighian tubules is unknown. Hypotheses include carbonic anhydrase activity, calcium and metal cation sequestration, and xenobiotic transport. This work presents the first comparative transcriptomic analysis of the Phasmatodean excretory organs, using the model insect Carausius morosus. I produced de novo transcriptomes of the midgut appendices, midgut wall, and Malpighian tubules, and looked for differentially expressed genes associated with putative organ functions. The appendices differentially and highly express lipid transport and metabolism proteins, and the biomineralization gene otopetrin. The Malpighian tubules differentially and highly express acid phosphatases and multiple transporter types, while appendices express fat-soluble vitamin and peptide transporters. Many defense proteins such as multidrug resistance proteins, ABC transporters, cytochrome P450's, and glutathione-S-transferases were differentially expressed in specific excretory organs. I hypothesize that the appendices and Malpighian tubules both have defensive / xenobiotic metabolism functions, but each likely target different substrates. Phasmid Malpighian tubules excrete as in other insects, while the appendices may predominantly regulate amino acids, fats, and fat-soluble compounds. Lipid metabolism in insects is poorly understood, and the Phasmatodea may thus serve as a model for studying this further.
Multiple Functions of Malpighian Tubules in Insects: A Review
Insects
The Malpighian Tubules (MTs) are the main excretory organs in most insects. They play a key role in the production of primary urine and osmoregulation, selectively reabsorbing water, ions, and solutes. Besides these functions conserved in most insects, MTs can serve some specialized tasks at different stages of some species’ development. The specialized functions include the synthesis of mucopolysaccharides and proteins for the building of foam nests, mucofibrils for the construction of dwelling tubes, adhesive secretions to help the locomotion, and brochosomes for protection as well as the usage of inorganic salts to harden the puparia, eggs chorion, and pupal cells’ closing lids. MTs are also the organs responsible for the astonishing bioluminescence of some Diptera glowworms and can go through some drastic histological changes to produce a silk-like fiber utilized to spin cocoons. The specialized functions are associated with modifications of cells within the entire tubules, in s...
Microscopic anatomy of pycnogonida: II. Digestive system. III. Excretory system
Journal of Morphology, 2007
The digestive system of several species of sea spiders (Pycnogonida, Arthropoda) was studied by electron microscopy. It is composed of the foregut inside a long proboscis, a midgut and a hindgut. Lips near the three jaws at the tip of the proboscis receive several hundred ductules originating from salivary glands. These previously undetected glands open on the lips, a fluted, projecting ridge at the external hinge line of the jaws, i.e., to the outside of the mouth. This disposition suggests affinities to the chelicerate line. The trigonal esophagus within the proboscis contains a complex, setose filter device, operated by dedicated muscles, that serves to reduce ingested food to subcellular dimensions. The midgut has diverticula into the bases of all legs. Its cells differentiate from the basal layer and contain a bewildering array of secretion droplets, lysosomes and phagosomes. In the absence of a hepatopancreas, the midgut serves both digestive and absorptive functions. The cuticle-lined hindgut lies in the highly reduced, peglike abdomen.
Cejkaian tubules' in the posterior midgut of terrestrial Enchytraeidae (Oligochaeta)
More than one hundred years ago, Bohumil Čejka described peculiar elongate tubules in the posterior region of the intestine of Hepatogaster birulae, a new terrestrial enchytraeid species collected in NorthEast Siberia. The tubules have no cilia but a proper epithelium and they run parallel to the longitudinal axis of the intestine over several segments, inside the intestinal epithelium but in close contact with the blood sinus. The tubules end blindly anteriorly and with a porus to the intestinal lumen posteriorly. The number of tubules increases from posterior to anterior due to bifurcations, and their diameter decreases. Čejka hypothesized that these tubules are glands that provide secretions for the final process of digestion or that aid in the egestion of faeces. He found them only in one species, Hepatogaster birulae, which was later synonymized with Henlea ochracea. In recent years we screened a large number of terrestrial enchytraeids in vivo and found these peculiar tubules ...
2000
Malpighian tubules proper are connected to the gut by ducts called trunks, the organization of which is described at ultrastructural level in the nymphs of various mayfly species, namely Ecdyonurus venosus (Heptageniidae), Ephemerella ignita (Ephemerellidae), Choroterpes picteti (Leptophlebiidae), and Caenis luctuosa (Caenidae). Trunks are luminal tubes varying in arrangement, number, shape, and length. The main cell type of the trunk wall is represented by cells that are bordered by a thin cuticle along their luminal side (type-A cells). Whereas these cells are exclusive in the long trunks (such as those of C. picteti and C. luctuosa), in the shorter ones (such as those of E. venosus and Ephemerella ignita) cells with a microvillous luminal border (type-B cells) are also encountered. These cells are located close to the entrance of the collecting duct of the Malpighian tubules proper, and their long microvilli form a dense filamentous mesh filling up the lumen. Both cell types exhibit fine structural features that are characteristics of ion-transporting epithelia. Ultrastructural investigations show that trunks are not a simple conducting system but are involved in the regulation of the ionic composition of the primary urine for producing a fluid hypo-osmotic with respect to the hemolymph.
Phylogenetic considerations of insect digestion
Insect Biochemistry, 1985
Amylase, cellobmse, cellulase, trehalase and trypsin are found m major amounts m the mldgut lumen, whereas ammopeptldase (winch J~ membrane bound) occurs mainly m the mldgut ttssue of Tenebrw mohtor larvae Cellulase and a minor ammopeptldase seem to be derived from fung~ contarmnatmg the wheat bran used as food The data suggest that the majority of carbohydrate digestion should take place m the lumen of anterior midgut, whereas protein &gestlon should occur partly m the lumen and partly at the cell surface of the postenor mldgut The finding that less than 5% of the total amylase, celloblase, maltase and trypsin are excreted, after a ume ~dent~cal to the passage time of the food bolus, leads to the proposal that there erasts an endo--ectoperttrophic ctrculatlon of enzymes by winch these enzymes are recovered from the undigested food before it is excreted There is only one molecular specms of cellobmse (pH opUmum 5 3, K m 1 1 mM, pI 3 7, M r 75,000), maltase (pH opttmum 5 3, Km 3 7 mM, pI 3 6, Mr 60,000) and trehalase (pH optimum 5 0, Km 0 40 mM, pI 4 0, M r 60,000) m T mohtor larval mldguts as judged by electrophoretlc, lsoelectnc focusing and density-gradient centnfugaUon data The data led to the proposal that &mer and oligomer hydrolases are small in Coleoptera ancestors and large m Diptera and Lepldoptera ancestors For tins, the majority of T mohtor larval &gestaon takes place reside the perltropinc membrane, whereas m Rhynchoscmra americana (Diptera) and Ermnyts ello (Lepldoptera) larvae lmtial &gestlon occurs mstde and intermediate and final &gestton outside the pentropinc membrane Key Word Index Digestion and phylogeny, mealworm celloinase, mealworm maltase, mealworm trehalase, excretion of enzymes, conversaUon of enzymes, permeability of the pentropinc membrane, evoluuon of digestion
Arthropod Structure & Development, 2004
Hemipterans are characterized by the absence of the peritrophic membrane, an anatomical structure that envelopes the food bolus in the majority of insects. However, the microvillar membranes of many hemipteran midgut cells are not in direct contact with the food bolus, due to the existence of the so-called perimicrovillar membrane (PMM), which covers the microvilli extending into the gut lumen with dead ends. a-Glucosidase is a biochemical marker for PMM in the seed sucker bug Dysdercus peruvianus (Heteroptera: Pyrrhocoridae). In this article, we report that adults of the major hemipteran infra-orders (Sternorrhyncha, Auchenorrhyncha, and Heteroptera) have PMM and a major membrane bound a-glucosidase, which has properties similar to those of the D. peruvianus enzyme. A polyclonal antibody raised against the enzyme of D. peruvianus recognized the enzymes present in PMM from the above-mentioned hemipteran groups. The same antibody was also able of recognizing perimicrovillar a-glucosidase from thrips. No PMM nor membrane-bound a-glucosidase were found in Psocoptera and Phthiraptera midguts. This suggests that PMM and PMM-bound-a-glucosidase are widespread among insects of the order Hemiptera and of the sister order Thysanoptera. The data support the hypothesis that PMM may have originated in the Condylognatha (Paraneopteran taxon including Hemiptera and Thysanoptera) ancestral stock and are associated with plant sap feeding. q
Evolutionary trends of digestion and absorption in the major insect orders
Arthropod Structure & Development, 2020
The spatial organization of digestion, which corresponds to the steps by which the ingested food is hydrolyzed in the different regions of the gut, was described in insects from the major insect orders. The pattern of digestion and absorption in the midgut shows a strong phylogenetic influence, modulated by adaptation to particular feeding habits. Based on this, basic digestive patterns were recognized and were proposed to represent the major ancestors from which the different orders evolved. The putative ancestors chosen to represent different points in the evolution from basal Neoptera to more derived orders were: Neoptera, Polyneoptera, Hemiptera, Hymenoptera-Panorpoidea (Diptera-Lepidoptera), Lepidoptera, and Cyclorrhapha. The basic plan of Neoptera was supposed to be alike that of Polyneoptera, which was hypothesized from studies performed in grasshoppers, crickets and from stick insects. For Holometabola, the basic plan was initially proposed from studies carried out in beetles, bees, nematocerous flies, common flies and also from moths. This review updates the physiological data supporting the putative midgut basic patterns by discussing available data on insects pertaining to different taxa and details the evolutionary trends of midgut function among the major insect orders. Furthermore, by using recent genomic and transcriptome data, this review discusses the few insects for which the spatial organization of midgut absorption is known.
Ultrastructure and secretory activity of Abracris flavolineata (Orthoptera: Acrididae) midguts
Journal of Insect Physiology, 1997
The midgut of Abracris Jlavofineatu adults comprises a ventriculus and six anteriorly placed caeca each displaying an anterior and a posterior lobe. Columnar cells in the caeca and anterior ventriculus present secretory vesicles originating from abundant Golgi areas, which seem to result (through exocytosis) in dark granules among the microvilli. A. Jlavolineatu males were starved for 24 h, fed for 20 min at noon and dissected at 0, 1, 3 and 5 h after the meal.