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Morphophysiological study of digestive system litter-feeding termite Cornitermes cumulans (Kollar, 1832)

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Abstract

Termites are the major decomposers of lignocellulosic biomass on Earth and are commonly considered as biological reactor models for lignocellulose degradation. Despite their biotechnological potential, few studies have focused on the morphophysiological aspects of the termite digestive system. We therefore analyze the morphology, ultrastructure and gut luminal pH of the digestive system in workers of the litter-feeding termite Cornitermes cumulans (Blattodea: Termitidae). Their digestive system is composed of salivary glands and an alimentary canal with a pH ranging from neutral to alkaline. The salivary glands have an acinar structure and present cells with secretory characteristics. The alimentary canal is differentiated into the foregut, midgut, mixed segment and hindgut, which comprises the ileum (p1), enteric valve (p2), paunch (p3), colon (p4) and rectum (p5) segments. The foregut has a well-developed chewing system. The midgut possesses a tubular peritrophic membrane and two cell types: digestive cells with secretory and absorptive features and several regenerative cells in mitosis, both cell types being organized into regenerative crypts. The mixed segment exhibits cells rich in glycogen granules. Hindgut p1, p4 and p5 segments have flattened cells with a few apical invaginations related to mitochondria and a thick cuticular lining. Conversely, the hindgut p3 segment contains large cuboid cells with extensive apical invaginations associated with numerous mitochondria. These new insights into the morphophysiology of the digestive system of C. cumulans reveal that it mobilizes lignocellulose components as a nutritional source by means of a highly compartmentalized organization with specialized segments and complex microenvironments.

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References

  • Baldrian P, Valášková V (2008) Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 32:501–521

    Article  CAS  PubMed  Google Scholar 

  • Baumann O, Walz B (2012) The blowfly salivary gland— a model system for analyzing the regulation of plasma membrane V-ATPase. J Insect Physiol 58:450–458

  • Bignell DE (1994) Soil-feeding and gut morphology in higher termites. In: Hunt JH, Nalepa CA (eds) Nourishment and evolution in insect societies. Westview, Boulder, pp 131–159

    Google Scholar 

  • Bignell DE, Eggleton P (1995) On the elevated intestinal pH of higher termites (Isoptera: Termitidae). Insect Soc 42:57–69

    Article  Google Scholar 

  • Bignell DE, Oskarsson H, Anderson JM (1980) Specialization of the hindgut wall for the attachment of symbiotic micro-organisms in a termite Procubitermes aburiensis (Isoptera, Termitidae, Termitinae). Zoomorphology 96:103–112

    Article  Google Scholar 

  • Bignell DE, Oskarsson H, Anderson JM, Ineson P, Wood TG (1983) Structure, microbial associations and function of the so-called “mixed segment” of the gut in two soil-feeding termites, Procubitermes aburiensis and Cubitermes severus (Termitidae, Termitinae). J Zool 201:445–480

    Article  Google Scholar 

  • Billingsley PF (1990) The midgut ultrastructure of hematophagous insects. Annu Rev Entomol 35:219–248

    Article  Google Scholar 

  • Breznak JA, Pankratz HS (1977) In situ morphology of the gut microbiota of wood-eating termites [Reticulitermes flavipes (Kollar) and Coptotermes formosanus Shiraki]. Appl Environ Microbiol 33:406–426

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brune A (2014) Symbiotic digestion of lignocellulose in termite guts. Nat Rev Microbiol 12:168–180

    Article  CAS  PubMed  Google Scholar 

  • Brune A, Dietrich C (2015) The gut microbiota of termites: digesting the diversity in the light of ecology and evolution. Annu Rev Microbiol 69:145–166

    Article  CAS  PubMed  Google Scholar 

  • Brune A, Friedrich M (2000) Microecology of the termite gut: structure and function on a microscale. Curr Opin Microbiol 3:263–269

    Article  CAS  PubMed  Google Scholar 

  • Brune A, Kühl M (1996) pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes. J Insect Physiol 42:1121–1127

    Article  CAS  Google Scholar 

  • Brune A, Emerson D, Breznak JA (1995) The termite gut microflora as an oxygen sink: microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Appl Environ Microbiol 61:2681–2687

    CAS  PubMed  PubMed Central  Google Scholar 

  • Constantino R (2002) The pest termites of South America: taxonomy, distribution and status. J Appl Entomol 126:355–365

    Article  Google Scholar 

  • De Sousa G, Conte H (2013) Midgut morphophysiology in Sitophilus zeamais Motschulsky, 1855 (Coleoptera: Curculionidae). Micron 51:1-8

  • De Sousa G, Scudeler EL, Abrahao J, Conte H (2013) Functional Morphology of the Crop and Proventriculus of Sitophilus zeamais (Coleoptera: Curculionidae). Annals of the Entomological Society of America 106 (6):846-852

  • Donovan SE, Eggleton P, Bignell DE (2001) Gut content analysis and a new feeding group classification of termites. Ecol Entomol 26:356–366

    Article  Google Scholar 

  • Eggleton P (2011) An introduction to termites: biology, taxonomy and functional morphology. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 1–26

    Google Scholar 

  • Fernandes PM, Alves SB (1992) Preferência alimentar e danos de Cornitermes cumulans (Kollar 1832) (Isoptera: Termitidae) às plantas cultivadas em laboratório. An Soc Entomol Brasil 21:125–132

    Google Scholar 

  • Fernandes PM, Czepak C, Veloso VRS (1998) Cupins de montículos em pastagens: prejuízo real ou praga estética? In: Fontes LR, Berti-Filho E (eds) Cupins: o desafio do conhecimento. FEALQ, Piracicaba, pp 187–210

    Google Scholar 

  • Fujita A, Miura T, Matsumoto T (2008) Differences in cellulose digestive systems among castes in two termite lineages. Physiol Entomol 33:73–82

    Article  CAS  Google Scholar 

  • Gomes FM, Carvalho DB, Machado EA, Miranda K (2013) Ultrastructural and functional analysis of secretory goblet cells in the midgut of the lepidopteran Anticarsia gemmatalis. Cell Tissue Res 352:313–326

    Article  CAS  PubMed  Google Scholar 

  • Grosse AS, Pressprich MF, Curley LB, Hamilton KL, Margolis B, Hildebrand JD, Gumucio DL (2011) Cell dynamics in fetal intestinal epithelium: implications for intestinal growth and morphogenesis. Development 138:4423–4432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jouquet P, Traoré S, Choosai C, Hartmann C, Bignell D (2011) Influence of termites on ecosystem functioning. Ecosystem services provided by termites. Eur J Soil Biol 47:215–222

    Article  Google Scholar 

  • Junqueira LCU, Junqueira LMMS (1983) Técnicas básicas de citologia e histologia. Santos, São Paulo

    Google Scholar 

  • Kappler A, Brune A (1999) Influence of gut alkalinity and oxygen status on mobilization and size-class distribution of humic acids in the hindgut of soil-feeding termites. Appl Soil Ecol 13:219–229

    Article  Google Scholar 

  • Klowden MJ (2007) Physiological systems in insects. Elsevier/Academic Press, Amsterdam

    Google Scholar 

  • Köhler T, Dietrich C, Scheffrahn RH, Brune A (2012) High-resolution analysis of gut environment and bacterial microbiota reveals functional compartmentation of the gut in wood-feeding higher termites (Nasutitermes spp.). Appl Environ Microbiol 78:4691–4701

    Article  PubMed  PubMed Central  Google Scholar 

  • Korb J (2011) Termite mound architecture, from function to construction. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 349–373

    Google Scholar 

  • Kumara RP, Saitoh S, Aoyama H, Shinzato N, Tokuda G (2015) Predominant expression and activity of vacuolar H+-ATPases in the mixed segment of the wood-feeding termite Nasutitermes takasagoensis. J Insect Physiol 78:1–8

    Article  CAS  PubMed  Google Scholar 

  • Kumara RP, Saitoh S, Aoyama H, Shinzato N, Tokuda G (2016) Metabolic pathways in the mixed segment of the wood-feeding termite Nasutitermes takasagoensis (Blattodea (Isoptera): Termitidae). Appl Entomol Zool 51:429–440

    Article  CAS  Google Scholar 

  • Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P, Hammel KE, Wymelenberg AV, Gaskell J, Lindquist E, Sabat G, BonDurant SS, Larrondo LF, Canessa P, Vicuna R, Yadav J, Doddapaneni H, Subramanian V, Pisabarro AG, Lavín JL, Oguiza JA, Master E, Henrissat B, Coutinho PM, Harris P, Magnuson JK, Baker SE, Bruno K, Kenealy W, Hoegger PJ, Kües U, Ramaiya P, Lucas S, Salamov A, Shapiro H, Tu H, Chee CL, Misra M, Xie G, Teter S, Yaver D, James T, Mokrejs M, Pospisek M, Grigoriev IV, Brettin T, Rokhsar D, Berka R, Cullenf D (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci U S A 106:1954–1959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nardi JB, Bee CM (2012) Regenerative cells and the architecture of beetle midgut epithelia. J Morphol 273:1010–1020

    Article  PubMed  Google Scholar 

  • Nardi JB, Bee CM, Miller LA (2010) Stem cells of the beetle midgut epithelium. J Insect Physiol 56:296–303

    Article  CAS  PubMed  Google Scholar 

  • Neves PJ, Alves SB (1999) Controle associado de Cornitermes cumulans (Kollar 1832) (Isoptera: Termitidae) com Metarhizium anisopliae, Beauveria bassiana e imidacloprid. Sci Agric 56:305–311

    Article  Google Scholar 

  • Ni J, Tokuda G (2013) Lignocellulose-degrading enzymes from termites and their symbiotic microbiota. Biotechnol Adv 31:838–850

    Article  CAS  PubMed  Google Scholar 

  • Noirot C, Noirot-Timothée C (1977) Fine structure of the rectum in termites (Isoptera): a comparative study. Tissue Cell 9:693–710

    Article  CAS  PubMed  Google Scholar 

  • Novaretti WRT, Fontes LR (1998) Cupins: uma grave ameaça à cana-de-açúcar no nordeste de Brasil. In: Fontes LR, Berti-Filho E (eds) Cupins: o desafio do conhecimento. FEALQ, Piracicaba, pp 163–172

    Google Scholar 

  • Ohkuma M (2003) Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biotechnol 61:1–9

    Article  CAS  PubMed  Google Scholar 

  • Rein J, Voss M, Blenau W, Walz B, Baumann O (2008) Hormone-induced assembly and activation of V-ATPase in blowfly salivary glands is mediated by protein kinase A. Am J Physiol Cell Physiol 294:C56–C65

    Article  CAS  PubMed  Google Scholar 

  • Rouland-Lefèvre C (2011) Termites as pests of agriculture. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 499–517

    Google Scholar 

  • Santos VC, Araujo RN, Machado LAD, Pereira MH, Gontijo NF (2008) The physiology of the midgut of Lutzomyia longipalpis (Lutz and Neiva 1912): pH in different physiological conditions and mechanisms involved in its control. J Exp Biol 211:2792–2798

    Article  CAS  PubMed  Google Scholar 

  • Scudeler EL, Santos DC (2013) Effects of neem oil (Azadirachta indica A. Juss) on midgut cells of predatory larvae Ceraeochrysa claveri (Navás, 1911) (Neuroptera: Chrysopidae). Micron 44:125–132

    Article  CAS  PubMed  Google Scholar 

  • Sumner JP, Dow JA, Earley FG, Klein U, Jäger D, Wieczorek H (1995) Regulation of plasma membrane V-ATPase activity by dissociation of peripheral subunits. J Biol Chem 270:5649–5653

    Article  CAS  PubMed  Google Scholar 

  • Terra WR (1988) Physiology and biochemistry of insect digestion: an evolutionary perspective. Braz J Med Biol Res 21:657–734

    Google Scholar 

  • Terra WR, Ferreira C (1994) Insect digestive enzymes: properties, compartmentalization and function. Comp Biochem Physiol B 109:1–62

    Article  Google Scholar 

  • Tokuda G, Watanabe H (2007) Hidden cellulases in termites: revision of an old hypothesis. Biol Lett 3:336–339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tokuda G, Watanabe H, Matsumoto T, Noda H (1997) Cellulose digestion in the wood-eating higher termite, Nasutitermes takasagoensis (Shiraki): distribution of cellulases and properties of endo-β-1,4-glucanase. Zool Sci 14:83–93

    Article  CAS  PubMed  Google Scholar 

  • Tokuda G, Lo N, Watanabe H, Slaytor M, Matsumoto T, Noda H (1999) Metazoan cellulase genes from termites: intron/exon structures and sites of expression. Biochim Biophys Acta 1447:146–159

    Article  CAS  PubMed  Google Scholar 

  • Tokuda G, Yamaoka I, Noda H (2000) Localization of symbiotic Clostridia in the mixed segment of the termite Nasutitermes takasagoensis (Shiraki). Appl Environ Microbiol 66:2199–2207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tokuda G, Nakamura T, Murakami R, Yamaoka I (2001) Morphology of the digestive system in the wood-feeding termite Nasutitermes takasagoensis (Shiraki) [Isoptera: Termitidae]. Zool Sci 18:869–877

    Article  Google Scholar 

  • Tokuda G, Lo N, Watanabe H, Arakawa G, Matsumoto T, Noda H (2004) Major alteration of the expression site of endogenous cellulases in members of an apical termite lineage. Mol Ecol 13:3219–3228

    Article  CAS  PubMed  Google Scholar 

  • Tokuda G, Miyagi M, Makiya H, Watanabe H, Arakawa G (2009) Digestive β-glucosidases from the wood-feeding higher termite, Nasutitermes takasagoensis: intestinal distribution, molecular characterization, and alteration in sites of expression. Insect Biochem Mol Biol 39:931–937

    Article  CAS  PubMed  Google Scholar 

  • Tokuda G, Watanabe H, Hojo M, Fujita A, Makiya H, Miyagi M, Arakawa G, Arioka M (2012) Cellulolytic environment in the midgut of the wood-feeding higher termite Nasutitermes takasagoensis. J Insect Physiol 58:147–154

    Article  CAS  PubMed  Google Scholar 

  • Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We express our gratitude to Diogo Gama dos Santos for his help with termite collection; the Rudolph Barth Electron Microscopy Platform at the Oswaldo Cruz Foundation, Rio de Janeiro, Brazil, for access to the transmission electron microscope used in this work; the National Center for Structural Biology and Bio-imaging at the Federal University of Rio de Janeiro, Rio de Janeiro, Brazil, for access to the stereo zoom microscope used in the immunohistochemical analysis; and the NIH Fellows Editorial Board for editorial assistance. This work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

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Correspondence to Ednildo de Alcantara Machado.

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de Sousa, G., dos Santos, V.C., de Figueiredo Gontijo, N. et al. Morphophysiological study of digestive system litter-feeding termite Cornitermes cumulans (Kollar, 1832). Cell Tissue Res 368, 579–590 (2017). https://doi.org/10.1007/s00441-017-2584-1

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