Alexandre Lobo-da-Cunha

Gianluca Tettamanti

Morena Casartelli

Frontiers in Physiology

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Editorial: Molecular physiology ofinvertebrate digestive systemAlexandre Lobo-da-Cunha1*, Morena Casartelli2* andGianluca Tettamanti3*1Department of Microscopy, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto,Porto, Portugal, 2Department of Biosciences, University of Milano, Milano, Italy, 3Department ofBiotechnology and Life Sciences, University of Insubria, Varese, ItalyKEYWORDSinsects, extracellular digestion, intracellular digestion, gut microbiota, digestivemetabolismEditorial on the Research TopicMolecular physiology of invertebrate digestive systemInvertebrate animals occur in all aquatic and terrestrial habitats from deep-sea to deserts,far outnumbering vertebrates and exceeding them in biological diversity, being essential forecosystem functioning and services (Laumer et al., 2019; Eisenhauer and Hines, 2021).Invertebrates range in size frommicroscopic rotifers to giant squids, feed on a huge variety offood sources, and some evolved to become efficient parasites. Their digestive systems reflectthis diversity. Animal wellbeing and performance rely on organic nutrients, with thedigestive system playing a pivotal role in processing food and providing the body withmolecules. These molecules are either utilized for energy or serve as essential substrates forvarious biosynthetic processes (Karasov and Douglas, 2013). Nevertheless, this is not true forall metazoans because some invertebrates lack a digestive system. In these cases, the digestivesystem is functionally replaced by other structures [e.g., the integument in parasitic worms(Dalton et al., 2004)], or by symbiotic chemoautotrophy microorganisms which supplynutrients to their host as in the case of adults of deep-sea hydrothermal vent tubeworms(Bright and Lallier, 2010). Other invertebrates lacking the digestive system can be foundamong sponges, placozoans, and bivalves (Gustafson and Reid, 1988). For example, mostsponges simply capture microscopic organic particles suspended in water by phagocytosis orendocytosis and digest them into choanocytes, relying entirely on intracellular digestiveprocesses. In placozoans, the lipophilic cells of the ventral epithelium secrete digestiveenzymes over algae and then the absorptive cells collect products of external digestion byendocytosis for further breakdown in lysosomes. A true digestive compartment can be foundfor the first time in cnidarians, which have a simple digestive system consisting of a singleopening that leads to a gastrovascular cavity where extracellular digestion takes place byaction of secreted enzymes (Steinmetz, 2019).Much more complex digestive systems consisting of a tubular digestive tract associatedwith glands that secrete enzymes for extracellular digestion can be found in Bilateria. Amonginvertebrates, the most elaborate digestive systems with complex mouthparts adapted to alarge variety of feeding strategies can be observed in molluscs and arthropods. In molluscs,although extracellular digestion and absorption can start in the foregut, most of digestion,absorption, and storage of reserves occur in the diverticula of the digestive gland. In thisorgan, basophilic cells are specialized in secretion of enzymes for extracellular digestion,while digestive cells collect products of extracellular digestion by endocytosis to complete theOPEN ACCESSEDITED AND REVIEWED BYSylvia Anton,Institut National de recherche pourl’agriculture, l’alimentation etl’environnement (INRAE), France*CORRESPONDENCEAlexandre Lobo-da-Cunha,alcunha@icbas.up.ptMorena Casartelli,morena.casartelli@unimi.itGianluca Tettamanti,Gianluca.Tettamanti@uninsubria.itRECEIVED 30 September 2023ACCEPTED 03 October 2023PUBLISHED 11 October 2023CITATIONLobo-da-Cunha A, Casartelli M andTettamanti G (2023), Editorial: Molecularphysiology of invertebratedigestive system.Front. Physiol. 14:1304915.doi: 10.3389/fphys.2023.1304915COPYRIGHT© 2023 Lobo-da-Cunha, Casartelli andTettamanti. This is an open-access articledistributed under the terms of theCreative Commons Attribution License(CC BY). The use, distribution orreproduction in other forums ispermitted, provided the original author(s)and the copyright owner(s) are creditedand that the original publication in thisjournal is cited, in accordance withaccepted academic practice. No use,distribution or reproduction is permittedwhich does not comply with these terms.Frontiers in Physiology frontiersin.org01TYPE EditorialPUBLISHED 11 October 2023DOI 10.3389/fphys.2023.1304915digestion in lysosomes (Lobo-da-Cunha, 2019). In general,arthropods and other ecdysozoans rely mostly on extracellulardigestion to obtain simple molecules that are transported throughthe absorbing epithelial cells which are characterized by a denseapical brush border (Steinmetz, 2019). In decapod crustaceans thehepatopancreas is the major digestive organ, with F cells responsiblefor secretion of digestive enzymes and R cells that absorb nutrients.The precise function of B cells, another cell type within this organ,remains unclear. There has been a hypothesis suggesting that thesecells might play a role in lipid digestion (Vogt, 2019). In insects, thelargest and most diverse group of organisms on Earth which hasbeen able to exploit an extraordinary range of ecological niches anddiets, the digestive system basically consists of a tube running fromthe mouth to the anus, but remarkable morphofunctionaldifferentiation can be observed among different species accordingto the nutritional quality and the texture of the food (Dow, 1986).The alimentary canal is organized in three main regions withdifferent features, functions, and embryonic origin (i.e., theforegut, the midgut, and the hindgut), where the midgut carriesout food digestion and nutrient absorption. In particular, columnarcells, the predominant cell type in this gut region, are responsible fordigestive enzyme production and absorption of nutrients (Cacciaet al., 2019). The microbiota associated to the insect gut has animportant impact on the physiology of these organisms as itcontributes to the host fitness by supplying essential nutrients,supporting food digestion and degradation of ingested toxicmolecules, and modulating defense mechanisms (Engel andMoran, 2013; Douglas, 2015; Jing et al., 2020).In insects and other invertebrates, the digestive system servesnot only for the digestion and absorption of nutrients but also plays arole in defense against pathogens (Zeng et al., 2022). Additionally, itis equipped with enteroendocrine and nervous cells that participatein regulating feeding and digestion, as well as modulatingcommunication between the alimentary canal and other organs(Wegener and Veenstra, 2015; García-Arrarás et al., 2019;Tierney, 2020).Despite a wide literature on this topic, information is stillfragmentary and much remains to be investigated about thephysiology of invertebrate digestive systems, especially at cellularand molecular level. Hence, this Research Topic aimed at providingfresh knowledge on the subject. In this scenario, the study ofdigestive system of insects is of particular importance due totheir relevance as pests and disease vectors, but also aspollinators and protein source.The relevance of the gut microbiota in supporting nutritionalrequirement of the insect host is the object of two studies in thisResearch Topic. Qian et al. demonstrated that the microbiota, inparticular bacteria belonging to the phylum Saccharibacteria, playsan important role during diapause in the lepidopteran species Clanisbilineata tsingtauica as it supplies nutrient and regulates nutrientmetabolism, supporting the insect during this peculiar life period. Byusing a multi-omics approach Zhang et al. investigated how thefunctionality of gut microbiota facilitates the exploitation oflignocellulose in the larvae of the coleopteran Apriona swainsoni,which attack healthy trees and live inside main branches and trunks,causing high mortality in the host plant.The impact of feeding on native versus exotic host plant ondifferent physiological parameters was evaluated in an herbivorousinsect, the lepidopteran Junonia coenia, by Mo and Smilanich. Inparticular, the authors examined if and how feeding on differenthost plants affects immune response, development, and foodexploitation.The study by Van Lommel et al. compared the gene expressionprofile in the midgut of the desert locust, Schistocerca gregaria, atdifferent time points after feeding, shedding light on midgutfunctionality in this hemimetabolous insect.Finally, two studies deal with the kissing bug Rhodnious prolixus,a primary vector of Chagas disease and a model species for studyinginsect physiology, especially concerning blood digestion. A lot ofinformation is available in the literature on the mechanisms andregulation of protein digestion in this insect, but carbohydratesdigestion is far less studied. Gama et al. examined this aspect,studying the physiological role of fucosidase, one of the majorexoglycosidases in R. prolixus, and clarifying the mechanism ofits production after blood feeding. The second study, by Moraes et al.,demonstrated that RNAi silencing of acetyl-CoA carboxylase in the fatbody of R. prolixus adult females negatively affects digestion, synthesisof lipids, and reproduction. Since the ingested blood contains lowamount of lipids, this insect relies on amino acids derived from bloodproteins to synthesize lipids. The results of this study unravel a centralrole of de novo lipogenesis, and in particular of acetyl-CoA carboxylasewhich is the enzyme that catalyzes the first step of de novo synthesis offatty acid, in the fitness of this insect.Author contributionsAL-d-C: Writing–original draft, Writing–review and editing.MC: Writing–original draft, Writing–review and editing. GT:Writing–original draft, Writing–review and editing.FundingThe author(s) declare that no financial support was received forthe research, authorship, and/or publication of this article.Conflict of interestThe authors declare that the research was conducted in theabsence of any commercial or financial relationships that could beconstrued as a potential conflict of interest.The author(s) declared that they were an editorial boardmember of Frontiers, at the time of submission. This had noimpact on the peer review process and the final decision.Publisher’s noteAll claims expressed in this article are solely those of the authorsand do not necessarily represent those of their affiliatedorganizations, or those of the publisher, the editors and thereviewers. Any product that may be evaluated in this article, orclaim that may be made by its manufacturer, is not guaranteed orendorsed by the publisher.Frontiers in Physiology frontiersin.org02Lobo-da-Cunha et al. 10.3389/fphys.2023.1304915ReferencesBright, M., and Lallier, F. H. (2010). The biology of vestimentiferan tubeworms.Oceanogr. Mar. Biol. 48, 213–265. doi:10.1201/EBK1439821169-c4Caccia, S., Casartelli, M., and Tettamanti, G. (2019). The amazing complexity of insectmidgut cells: types, peculiarities, and functions. Cell Tissue Res. 377, 505–525. doi:10.1007/s00441-019-03076-wDalton, J. P., Skelly, P., and Halton, D.W. (2004). Role of the tegument and gut in nutrientuptake by parasitic platyhelminths. Can. J. Zool. 82, 211–232. doi:10.1139/z03-213Douglas, A. E. (2015). Multiorganismal insects: diversity and function of residentmicroorganisms. Annu. Rev. Entomol. 60, 17–34. doi:10.1146/annurev-ento-010814-020822Dow, J. A. T. (1986). Insect midgut function. Adv. 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Editorial: Molecular physiology of invertebrate digestive system

Lobo-da-Cunha, Alexandre

Casartelli, Morena

Tettamanti, Gianluca

Archivio istituzionale della ricerca - Università dell'Insubria

https://www.frontiersin.org/articles/10.3389/fphys.2023.1304915/pdf?isPublishedV2=False

Editorial: Molecular physiology of invertebrate digestive system

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