Hostname: page-component-76fb5796d-wq484 Total loading time: 0 Render date: 2024-04-26T05:54:43.963Z Has data issue: false hasContentIssue false
  • English
  • Français

Ultrastructure of the Bacteriocytes in the Midgut of the Carpenter ant Camponotus rufipes: Endosymbiont Control by Autophagy

Part of: Micrographia Collection

Published online by Cambridge University Press:  14 September 2020

Wagner G. Gonçalves ,
Kenner M. Fernandes ,
Ana Paula A. Silva ,
Danilo G. Gonçalves ,
Muhammad Fiaz  and
José Eduardo Serrão Open the ORCID record for José Eduardo Serrão [Opens in a new window]
Wagner G. Gonçalves
Affiliation:
Department of General Biology, Universidade Federal de Viçosa, Viçosa, Brazil
Kenner M. Fernandes
Affiliation:
Department of General Biology, Universidade Federal de Viçosa, Viçosa, Brazil
Ana Paula A. Silva
Affiliation:
Department of Entomology, Universidade Federal de Viçosa, Viçosa, Brazil
Danilo G. Gonçalves
Affiliation:
Department of Basic and Life Sciences, Universidade Federal de Juiz de Fora, Governador Valadares, Brazil
Muhammad Fiaz
Affiliation:
Department of Entomology, Universidade Federal de Viçosa, Viçosa, Brazil
José Eduardo Serrão*
Affiliation:
Department of General Biology, Universidade Federal de Viçosa, Viçosa, Brazil
*
*Author for correspondence: José Eduardo Serrão, E-mail: jeserrao@ufv.br
Get access

Abstract

The carpenter ant Camponotus rufipes has intracellular bacteria in bacteriocytes scattered in the midgut epithelium, which have different amounts of endosymbionts, according to the developmental stages. However, there are no detailed data about the midgut cells in adult workers. The present work aimed to evaluate the morphology and cellular events that coordinate the abundance of endosymbionts in the midgut cells in C. rufipes workers. The midgut epithelium has digestive cells, bacteriocytes, and cells with intermediate morphology. The latter is similar to bacteriocytes, due to the abundance of endosymbionts, and similar to digestive cells, due to their microvilli. The digestive and intermediate cells are rich in autophagosomes and autolysosomes, both with bacteria debris in the lumen. These findings suggest that midgut cells of C. rufipes control the endosymbiont level by the autophagy pathway.

Keywords

autophagyBlochmanniaFormicidaeinsectsymbiosis
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 26 , Issue 6 , December 2020 , pp. 1236 - 1244
Copyright
Copyright © Microscopy Society of America 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bancroft, JD & Gamble, M (2008). Theory and Practice of Histological Techniques. London: Churchill Livingstone.Google Scholar
Bolton, B (1996). A New General Catalogue of the Ants of the World. Cambridge: Harvard University Press.Google Scholar
Buchner, P (1965). Endosymbiosis of Animals with Plant Microorganisms. New York: Intersciences Publishers Inc.Google Scholar
Cossolin, JFS, Lopes, DRG, Martinez, LC, Santos, HCP, Fiaz, M, Pereira, MJB, Vivan, LM, Mantovani, HC & Serrão, JE (2020). Morphology and composition of the midgut bacterial community of Scaptocoris castanea perty, 1830 (Hemiptera: Cydnidae). Cell Tissue Res. https://doi.org/10.1007/s00441-020-03197-7CrossRefGoogle ScholarPubMed
Deretic, V & Levine, B (2009). Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5, 527–549.CrossRefGoogle ScholarPubMed
Feldhaar, H, Straka, J, Krischke, M, Berthold, K, Stoll, S, Mueller, MJ & Gross, R (2007). Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biol 5, 48.CrossRefGoogle ScholarPubMed
Nishikori, K, Kubo, T & Morioka, M (2009 b). Morph-dependent expression and subcellular localization of host serine carboxypeptidase in bacteriocytes of the pea aphid associated with degradation of the endosymbiotic bacterium Buchnera. Zool Sci 26, 415–420.CrossRefGoogle ScholarPubMed
Nishikori, K, Morioka, K, Kubo, T & Morioka, M (2009 a). Age- and morph-dependent activation of the lysosomal system and Buchnera degradation in aphid endosymbiosis. J Insect Physiol 55, 351–357.CrossRefGoogle ScholarPubMed
Peloquin, JJ, Miller, SG, Klotz, SA, Stouthammer, R, Davis, LR Jr. & Klotz, JH (2001). Bacterial endosymbionts from the genus Camponotus (Hymenoptera: Formicidae). Sociobiology 38, 695–708.Google Scholar
Ratzka, C, Gross, R & Feldhaar, H (2013). Gene expression analysis of the endosymbiont-bearing midgut tissue during ontogeny of the carpenter ant Camponotus floridanus. J Insect Physiol 59, 611–623.CrossRefGoogle ScholarPubMed
Reynolds, ES (1963). Use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17, 208–212.CrossRefGoogle ScholarPubMed
Sauer, C, Dudaczek, D, Hölldobler, B & Gross, R (2002). Tissue localization of the endosymbiotic bacterium “Candidatus Blochmannia floridanus” in adults and larvae of the carpenter ant Camponotus floridanus. Appl Environ Microbiol 68, 4187–4193.CrossRefGoogle ScholarPubMed
Schröder, D, Deppisch, H, Obermayer, M, Krohne, G, Stackebrandt, E, Hölldobler, B, Goebel, W & Gross, R (1996). Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): Systematics, evolution and ultrastructural characterization. Mol Microbiol 21, 479–489.CrossRefGoogle ScholarPubMed
Skidmore, IH & Hansen, AK (2017). The evolutionary development of plant-feeding insects and their nutritional endosymbionts. Insect Sci 24, 910–928.CrossRefGoogle ScholarPubMed
Souza, DJ, Bézier, A, Depoix, D, Drezen, JM & Lenoir, A (2009). Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus fellah. BMC Microbiol 9, 29.CrossRefGoogle ScholarPubMed
Stefanini, M, Demartino, C & Zamboni, L (1967). Fixation of ejaculated spermatozoa for electron microscopy. Nature 216, 173–174.CrossRefGoogle ScholarPubMed
Stoll, S, Feldhaar, H, Fraunholz, MJ & Gross, R (2010). Bacteriocyte dynamics during development of a holometabolous insect, the carpenter ant Camponotus floridanus. BMC Microbiol 10, 308.CrossRefGoogle ScholarPubMed
Vigneron, A, Masson, F, Vallier, A, Balmand, S, Rey, M, Vincent-Monégat, C, Aksoy, E, Aubailly-Giraud, E, Zaidman-Rémy, A & Heddi, A (2014). Insects recycle endosymbionts when the benefit is over. Curr Biol 24, 2267–2273.CrossRefGoogle ScholarPubMed
Wernegreen, JJ, Kauppinen, SN, Brady, SG & Ward, PS (2009). One nutritional symbiosis begat another: Phylogenetic evidence that the ant tribe camponotini acquired Blochmannia by tending sap-feeding insects. BMC Evol Biol 9, 292.CrossRefGoogle ScholarPubMed
Wolschin, F, Hölldobler, B, Gross, R & Zientz, E (2004). Replication of the endosymbiotic bacterium Blochmannia floridanus is correlated with the developmental and reproductive stages of its ant host. Appl Environ Microbiol 70, 4096–4102.CrossRefGoogle ScholarPubMed
Zientz, E, Beyaert, I, Gross, R & Feldhaar, H (2006). Relevance of the endosymbiosis of Blochmannia floridanus and carpenter ants at different stages of the life cycle of the host. Appl Environ Microbiol 72, 6027–6033.CrossRefGoogle ScholarPubMed