The gut microbiome mediates adaptation to scarce food in Coleoptera

. 2023 Nov 13 ; 18 (1) : 80. [epub] 20231113

Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37957741

Grantová podpora
R01 DE024463 NIDCR NIH HHS - United States
R01DE024463 NIH HHS - United States

Odkazy

PubMed 37957741
PubMed Central PMC10644639
DOI 10.1186/s40793-023-00537-2
PII: 10.1186/s40793-023-00537-2
Knihovny.cz E-zdroje

Beetles are ubiquitous cave invertebrates worldwide that adapted to scarce subterranean resources when they colonized caves. Here, we investigated the potential role of gut microbiota in the adaptation of beetles to caves from different climatic regions of the Carpathians. The beetles' microbiota was host-specific, reflecting phylogenetic and nutritional adaptation. The microbial community structure further resolved conspecific beetles by caves suggesting microbiota-host coevolution and influences by local environmental factors. The detritivore species hosted a variety of bacteria known to decompose and ferment organic matter, suggesting turnover and host cooperative digestion of the sedimentary microbiota and allochthonous-derived nutrients. The cave Carabidae, with strong mandibula, adapted to predation and scavenging of animal and plant remains, had distinct microbiota dominated by symbiotic lineages Spiroplasma or Wolbachia. All beetles had relatively high levels of fermentative Carnobacterium and Vagococcus involved in lipid accumulation and a reduction of metabolic activity, and both features characterize adaptation to caves.

Před aktualizací

PubMed

Zobrazit více v PubMed

Racovitza EG. 1907. Essai sur les problèmes biospéologiques. Biospeologica I. Archive De Zoologie Experimentale Et Generale, ser 4, 6, 371–488.

Poulson TL, White WB. The cave environment. Science. 1969;165:971–81. doi: 10.1126/science.165.3897.971. PubMed DOI

Riddle MR, Aspiras AC, Gaudenz K, Peuß R, Sung JY, Martineau B, Peavey M, Box AC, Tabin JA, McGaugh S, Borowsky R, Tabin CJ, Rohner N. Insulin resistance in cavefish as an adaptation to a nutrient-limited environment. Nature. 2018;555:647–51. doi: 10.1038/nature26136. PubMed DOI PMC

Culver DC, Pipan T. The Biology of caves and other subterranean habitats. Biology of Habitats Series. 2nd ed. Oxford Academic; 2019.

Moldovan O. 2012. Beetles. In Culver, D., White, W.B, editors, Encyclopedia of Caves, 2nd edition, Elsevier Academic Press, pp. 54–62.

Howarth FG, Moldovan OT. The ecological classification of Cave animals and their adaptations. In: Moldovan OT, Kovac L, Halse S, editors. Cave Ecology. Springer International Publishing; 2018. pp. 41–67.

Ribera I, Fresneda J, Bucur R, Izquierdo A, Vogler AP, Salgado JM, Cieslak A. Ancient origin of a western Mediterranean radiation of subterranean beetles. BMC Evol Biol. 2010;10:29. doi: 10.1186/1471-2148-10-29. PubMed DOI PMC

Ortiz M, Legatzki A, Neilson J, Fryslie B, Nelson WM, Wing RA, Soderlund CA, Pryor BM, Maier RM. Making a living while starving in the dark: metagenomic insights into the energy dynamics of a carbonate cave. ISME J. 2014;8:478–91. doi: 10.1038/ismej.2013.159. PubMed DOI PMC

Zhu H-Z, Zhang Z-F, Zhou N, Jiang C-Y, Wang B-J, Cai L, Liu S-J. Diversity, distribution and co-occurrence patterns of bacterial communities in a karst cave system. Front Microbiol. 2019;10:1726. doi: 10.3389/fmicb.2019.01726. PubMed DOI PMC

Engel P, Moran NA. The gut microbiota of insects - diversity in structure and function. FEMS Microbiol Rev. 2013;37:699–735. doi: 10.1111/1574-6976.12025. PubMed DOI

Dillon RJ, Dillon VM. The gut bacteria of insects: nonpathogenic interactions. Ann Rev Entomol. 2004;49:71–92. doi: 10.1146/annurev.ento.49.061802.123416. PubMed DOI

Douglas AE. Multiorganismal insects: diversity and function of resident microorganisms. Ann Rev Entomol. 2015;60:17–34. doi: 10.1146/annurev-ento-010814-020822. PubMed DOI PMC

Deleurance-Glaçon S. Recherches sur les coléoptères troglobies de la sous-famille des Bathysciinae. Ann De Spéléologie. 1964;19:573–80.

Paoletti MG, Mazzon L, Martinez-Sañudo I, Simonato M, Beggio M, Dreon AL, Pamio A, Brilli M, Dorigo L, Engel AS, Tondello A, Baldan B, Concheri G, Squartini A. A unique midgut-associated bacterial community hosted by the cave beetle Cansiliella Servadeii (Coleoptera: Leptodirini) reveals parallel phylogenetic divergences from universal gut-specific ancestors. BMC Microbiol. 2013;13:129. doi: 10.1186/1471-2180-13-129. PubMed DOI PMC

Latella L, Castioni A, Bignotto L, Salvetti E, Tor-Riani S, Felis GE. Exploring gut microbiota composition of the cave beetles Neobathyscia Pasai Ruffo, 1950 and Neobathyscia mancinii Jeannel, 1924 (Leiodidae; Cholevinae) Boll Mus Civ St Nat Verona Botanica Zoologia. 2017;41:3–24.

Dragomir G, Șerban A, Năstase G, Brezeanu AI. Wind Energy in Romania: a review from 2009 to 2016. Ren Sust Energ Revs. 2016;64:129–43. doi: 10.1016/j.rser.2016.05.080. DOI

Christiansen KA. Proposition pour la classification des animaux cavernicoles. Spelunca Mem. 1962;2:75–8.

Jeannel R. Monographie Des Bathysciinae. Archives de Zoologie Expérimentale et Générale. 1924;63:1–436.

Bolyen E, Rideout JR, Dillon MR, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7. doi: 10.1038/s41587-019-0209-9. PubMed DOI PMC

Morton JT, Marotz C, Washburne A, Silverman J, Zaramela LS, Edlund A, Zengler K, Knight R. Establishing microbial composition measurement standards with reference frames. Nat Comm. 2019;10:2719. doi: 10.1038/s41467-019-10656-5. PubMed DOI PMC

Kováč Ľ. Caves as Oligotrophic ecosystems. In: Moldovan OT, Kováč L, Halse S, editors. Cave Ecology. Springer International Publications; 2018. pp. 297–307.

Holmes AJ, Tujula NA, Holley M, Contos A, James JM, Rogers P, Gillings MR. Phylogenetic structure of unusual aquatic microbial formations in Nullarbor Caves, Australia. Environ Microbiol. 2001;3:256–64. doi: 10.1046/j.1462-2920.2001.00187.x. PubMed DOI

Chiciudean I, Russo G, Bogdan DF, Levei EA, Faur L, Hillebrand-Voiculescu A, Moldovan OT, Banciu HL. Competition-cooperation in the chemoautotrophic ecosystem of Movile Cave: first metagenomic approach on sediments. Environ Microbiome. 2022;17:44. doi: 10.1186/s40793-022-00438-w. PubMed DOI PMC

De Mandal S, Kumar CR. Dominant bacterial phyla in caves and their predicted functional roles in C and N cycle. BMC Microbiol. 2017;17:90. doi: 10.1186/s12866-017-1002-x. PubMed DOI PMC

Gómez Expósito R, Postma J, Raaijmakers JM, De Bruijn I. Diversity and activity of Lysobacter species from Disease suppressive soils. Front Microbiol. 2015;6:1243. doi: 10.3389/fmicb.2015.01243. PubMed DOI PMC

Brewer TE, Aronson EL, Arogyaswamy K, Billings SA, Botthoff JK, Campbell AN, Dove NC, Fairbanks D, Gallery RE, Hart SC, Kaye J, King G, Logan G, Lohse KA, Maltz MR, Mayorga E, O’Neill C, Owens SM, Packman A, Pett-Ridge J, Plante AF, Richter DD, Silver WL, Yang WH, Fierer N. Ecological and genomic attributes of Novel Bacterial Taxa that Thrive in Subsurface Soil Horizons. mBio. 2019;10:e01318–19. doi: 10.1128/mBio.01318-19. PubMed DOI PMC

Yun JH, Roh SW, Whon TW, Jung MJ, Kim MS, Park DS, Yoon C, Nam YD, Kim YJ, Choi JH, Kim JY, Shin NR, Kim SH, Lee WJ, Bae JW. Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl Environ Microbiol. 2014;80:5254–64. doi: 10.1128/AEM.01226-14. PubMed DOI PMC

Kolasa M, Ścibior R, Mazur MA, Kubisz D, Dudek K, Kajtoch L. How hosts taxonomy, trophy, and endosymbionts shape Microbiome Diversity in Beetles. Microb Ecol. 2019;78:995–1013. doi: 10.1007/s00248-019-01358-y. PubMed DOI PMC

Franzini PZ, Ramond JB, Scholtz CH, Sole CL, Ronca S, Cowan DA. The gut microbiomes of two Pachysoma MacLeay desert dung beetle species (Coleoptera: Scarabaeidae: Scarabaeinae) feeding on different diets. PLoS ONE. 2016;11:e0161118. doi: 10.1371/journal.pone.0161118. PubMed DOI PMC

Pramono AK, Sakamoto M, Iino T, Hongoh Y, Ohkuma M. Dysgonomonas termitidis sp. nov. isolated from the gut of the subterranean termite Reticulitermes Speratus. Int J Syst Evol Microbiol. 2015;65:681–5. doi: 10.1099/ijs.0.070391-0. PubMed DOI

Chen B, The BS, Sun C, Hu S, Lu X, Boland W, Shao Y. Biodiversity and Activity of the gut microbiota across the life history of the Insect Herbivore Spodoptera Littoralis. Sci Rep. 2016;6:29505. doi: 10.1038/srep29505. PubMed DOI PMC

Ebert KM, Arnold WG, Ebert PR, Merritt DJ. Hindgut Microbiota reflects different Digestive strategies in Dung Beetles (Coleoptera: Scarabaeidae: Scarabaeinae) Appl Environ Microbiol. 2021;87:e02100–20. doi: 10.1128/AEM.02100-20. PubMed DOI PMC

Vogel H, Shukla S, Engl T, Weiss B, Fischer R, Steiger S, Heckel DG, Kaltenpoth M, Vilcinskas A. The digestive and defensive basis of carcass utilization by the burying beetle and its microbiota. Nat Comm. 2017;8:15186. doi: 10.1038/ncomms15186. PubMed DOI PMC

Zheng X, Zhu Q, Zhou Z, Wu F, Chen L, Cao Q, Shi F. 2021. Gut bacterial communities across 12 Ensifera (Orthoptera) at different feeding habits and its prediction for the insect with contrasting feeding habits. PLoS ONE 16, e0250675. PubMed PMC

Liu W, Li Y, Guo S, Yin H, Lei C-L, Wang X-P. Association between gut microbiota and diapause preparation in the cabbage beetle: a new perspective for studying insect diapause. Sci Rep. 2016;6:38900. doi: 10.1038/srep38900. PubMed DOI PMC

Kudo R, Masuya H, Endoh R, Kikuchi T, Ikeda H. Gut bacterial and fungal communities in ground-dwelling beetles are associated with host food habit and habitat. ISME J. 2019;13:676–85. doi: 10.1038/s41396-018-0298-3. PubMed DOI PMC

Koštál V, Štětina T, Poupardin R, Korbelová J, Bruce AW. Conceptual framework of the eco-physiological phases of insect diapause development justified by transcriptomic profiling. PNAS. 2017;114:8532–7. doi: 10.1073/pnas.1707281114. PubMed DOI PMC

Socha R, Sula J, Zemek R. Feeding, drinking and digestive enzyme activities in long- and short-day females of Pyrrhocoris Apterus (Heteroptera) Physiol Entomol. 1997;22:161–9. doi: 10.1111/j.1365-3032.1997.tb01153.x. DOI

Bajgar A, Jindra M, Dolezel D. Autonomous regulation of the insect gut by circadian genes acting downstream of juvenile hormone signaling. PNAS. 2013;110:4416–21. doi: 10.1073/pnas.1217060110. PubMed DOI PMC

Landesman WJ, Zachary B, Freedman D, Nelson M. Seasonal, sub-seasonal and diurnal variation of soil bacterial community composition in a temperate deciduous forest. FEMS Microb Ecol. 2019;95:fiz002. doi: 10.1093/femsec/fiz002. PubMed DOI PMC

Fejér A, Moldovan OT. Population size and dispersal patterns for a Drimeotus (Coleoptera, Leiodidae, Leptodirini) cave population. Subt Biol. 2013;11:31–44.

Premalatha N, Gopal NO, Jose PA, Anandham R, Kwon S-W. Optimization of cellulase production by Enhydrobacter sp. ACCA2 and its application in biomass saccharification. Front Microbiol. 2015;6:1046. doi: 10.3389/fmicb.2015.01046. PubMed DOI PMC

Silver A, Perez S, Gee M, Xu B, Garg S, Will K, Gill A. 2021. Persistence of the ground beetle (Coleoptera: Carabidae) microbiome to diet manipulation. PLoS ONE 16, e0241529. PubMed PMC

Iorizzo M, Albanese G, Testa B, Ianiro M, Letizia F, Succi M, Tremonte P, D’Andrea M, Iaffaldano N, Coppola R. Presence of lactic acid bacteria in the intestinal tract of the Mediterranean trout (Salmo macrostigma) in its natural environment. Life. 2021;11:667. doi: 10.3390/life11070667. PubMed DOI PMC

Gupta AK, Rastogi G, Nayduch D, Sawant SS, Bhonde RR, Shouche YS. Molecular phylogenetic profiling of gut-associated bacteria in larvae and adults of flesh flies. Med Vet Entomol. 2014;28:345–54. doi: 10.1111/mve.12054. PubMed DOI

Shukla SP, Plata C, Reichelt M, Steiger S, Heckel D, Kaltenpoth M, Vilcinskas A, Vogel H. Microbiome-assisted carrion preservation Aids larval development in a burying beetle. PNAS. 2018;115:11274–9. doi: 10.1073/pnas.1812808115. PubMed DOI PMC

Chakraborty A, Ashraf MZ, Modlinger R, Synek J, Schlyter F, Roy A. Unravelling the gut bacteriome of Ips (Coleoptera: Curculionidae: Scolytinae): identifying core bacterial assemblage and their ecological relevance. Sci Rep. 2020;10:18572. doi: 10.1038/s41598-020-75203-5. PubMed DOI PMC

Passerini D, Coddeville M, Le Bourgeois P, Loubière P, Ritzenthaler P, Fontagné-Faucher C, Daveran-Mingot ML, Cocaign-Bousquet M. The carbohydrate metabolism signature of Lactococcus lactis strain A12 reveals its sourdough ecosystem origin. Appl Env Microbiol. 2013;79:5844–52. doi: 10.1128/AEM.01560-13. PubMed DOI PMC

Pechal JL, Benbow ME, Crippen TL, Tarone AM, Tomberlin JK. Delayed insect access alters carrion decomposition and necrophagous insect community assembly. Ecosphere. 2014;5:1–21. doi: 10.1890/ES14-00022.1. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...