Gut compartments and ovary bacterial symbionts of the Sunn pest

다국어 초록 (Multilingual Abstract)

The Sunn pest, Eurygaster integriceps (Hemiptera: Scutelleridae), is the severe pest of cereals, especially of wheat in many parts of the world. Many insect species, including the Sunn pest that feed solely on nutritionally restricted diets, harbor symbiotic microorganisms. In the current study, we isolated and identified the Sunn pest bacterial symbionts of gut fractions and ovary. The phylogenetic analysis indicated that Sunn pest gut bacterial symbionts are polyphyletic and contained a taxonomic diversity belonging to three different phyla, including Firmicutes, Tenericutes, and Proteobacteria. Firmicutes was represented by Enterococcus, Proteobacteria by Pantoea and Acetobacteraceae, and Tenericutes by Spiroplasma. We isolated and identified Enterococcus, Acetobacteraceae, Spiroplasma and Pantoea from Sunn pest different gut compartments, and Pantoea from ovaries. There was considerable overlap between recognized symbionts from the 2nd and 3rd midgut sections (Acetobacteraceae), the 4th midgut section and hindgut (Spiroplasma), and 4th midgut section and ovary (Pantoea). Niche heterogeneity within a microbial habitat of gut fractions resulted in colonizing and adaptation of various communities of symbionts in each fraction. The Sunn pest gut compartments and ovary symbionts have been demonstrated to be of multiple evolutionary origins. This diversity may be of great importance to the Sunn pest fitness and survival in various overwintering niches.

참고문헌 (Reference)

1 Su, L., "Variation in the gut microbiota of termites(Tsaitermes ampliceps)against different diets" 181 : 32-47, 2017

2 Christoph Vorburger, "The role of defensive symbionts in host-parasite coevolution" Wiley 93 (93): 1747-1764, 2018

3 Philipp Engel, "The gut microbiota of insects – diversity in structure and function" Oxford University Press (OUP) 37 (37): 699-735, 2013

4 Katie Fisher, "The ecology, epidemiology and virulence of Enterococcus" Microbiology Society 155 (155): 1749-1757, 2009

5 Ballinger, M. J., "The defensive Spiroplasma" 32 : 36-41, 2019

6 Raman Bansal, "The crypt-dwelling primary bacterial symbiont of the polyphagous pentatomid pest Halyomorpha halys (Hemiptera:Pentatomidae)" Oxford University Press (OUP) 43 (43): 617-625, 2014

7 Mohammad Mehrabadi, "The Sunn pest, Eurygaster integriceps Puton (Hemiptera: Scutelleridae) digestive tract: Histology, ultrastructure and its physiological significance" Elsevier BV 43 (43): 631-637, 2012

8 Christopher M. Taylor, "The Importance of Gut Symbionts in the Development of the Brown Marmorated Stink Bug, Halyomorpha halys (Stål)" Public Library of Science (PLoS) 9 (9): e90312-, 2014

9 Francisco González-Serrano, "The Gut Microbiota Composition of the Moth Brithys crini Reflects Insect Metamorphosis" Springer Science and Business Media LLC 79 (79): 960-970, 2020

10 Cristina Vilanova, "The Generalist Inside the Specialist: Gut Bacterial Communities of Two Insect Species Feeding on Toxic Plants Are Dominated by Enterococcus sp." Frontiers Media SA 7 : 1005-, 2016

11 Shifen Xu, "The Bacterial Flora Associated with the Polyphagous Aphid Aphis gossypii Glover (Hemiptera: Aphididae) Is Strongly Affected by Host Plants" Springer Science and Business Media LLC 79 (79): 971-984, 2020

12 Kafil, M., "Role of symbiotic bacteria in the growth and development of the Sunn pest, Eurygaster integriceps" 13 : 99-, 2013

13 Kaiwa, N., "Primary gut symbiont and secondary, Sodalis-allied symbiont in the scutellerid stinkbug Cantao ocellatus" 76 : 3486-3494, 2010

14 Sugio, A., "Plant-insect interactions under bacterial influence : ecological implications and underlying mechanisms" 66 : 467-478, 2015

15 Kuechler, S. M., "Phylogenetically diverse burkholderia associated with midgut crypts of spurge bugs, Dicranocephalus spp. (Heteroptera: Stenocephalidae)" 31 (31): 145-153, 2016

16 Masaya Watanabe, "Novel Strain of Spiroplasma Found in Flower Bugs of the Genus Orius (Hemiptera: Anthocoridae): Transovarial Transmission, Coexistence with Wolbachia and Varied Population Density" Springer Science and Business Media LLC 67 (67): 219-228, 2014

17 Hong Yang, "Niche heterogeneity determines bacterial community structure in the termite gut (Reticulitermes santonensis)" Wiley 7 (7): 916-932, 2005

18 Angela E. Douglas, "Multiorganismal Insects: Diversity and Function of Resident Microorganisms" Annual Reviews 60 (60): 17-34, 2015

19 Sayumi Oishi, "Morphogenesis and development of midgut symbiotic organ of the stinkbug Plautia stali (Hemiptera: Pentatomidae)" Springer Science and Business Media LLC 5 (5): 16-, 2019

20 Craig D. Soutar, "Molecular validation of clinical Pantoea isolates identified by MALDI-TOF" Public Library of Science (PLoS) 14 (14): e0224731-, 2019

21 Amiri, A., "Molecular identification of cysteine and trypsin protease, effect of different hosts on protease expression, and RNAi mediated silencing of cysteine protease in the Sunn pest" 91 (91): 189-209, 2016

22 Sambrook, J., "Molecular Cloning : A laboratory manual" Spring Harbor Laboratory Press 2001

23 Crotti, E., "Microsensors for the characterization of the insect gut environment" 275 : 012014-, 2019

24 Brune, A., "Life at the oxic-anoxic interface : microbial activities and adaptations" 24 : 691-710, 2000

25 Ömer Çelebi, "Investigation of the internal bacterial flora of Eurygaster integriceps (Hemiptera: Scutelleridae) and pathogenicity of the flora members" Springer Science and Business Media LLC 69 (69): 1365-1375, 2014

26 Xili Liang, "Insect symbionts as valuable grist for the biotechnological mill: an alkaliphilic silkworm gut bacterium for efficient lactic acid production" Springer Science and Business Media LLC 102 (102): 4951-4962, 2018

27 Ryu, J. H., "Innate immune homeostasis by the homeobox gene Caudal and commensal-gut mutualism in Drosophila" 319 : 777-782, 2008

28 Yoshida, K., "Influences of two coexisting endosymbionts, CI-inducing Wolbachia and male-killing Spiroplasma, on the performance of their host Laodelphax striatellus(Hemiptera : Delphacidae)" 9 : 8214-8224, 2019

29 Takahiro Hosokawa, "Infection prevalence of Sodalis symbionts among stinkbugs" Springer Science and Business Media LLC 1 (1): 5-, 2015

30 Mateos, M., "Independent origins of resistance or susceptibility of parasitic wasps to a defensive symbiont" 6 : 2679-2687, 2016

31 Rémi Eliautout, "Immune response and survival of Circulifer haematoceps to Spiroplasma citri infection requires expression of the gene hexamerin" Elsevier BV 54 (54): 7-19, 2016

32 Javier A. Ceja-Navarro, "Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee" Springer Science and Business Media LLC 6 (6): 7618-, 2015

33 Gregory P. Donaldson, "Gut biogeography of the bacterial microbiota" Springer Science and Business Media LLC 14 (14): 20-32, 2016

34 Bandani, A. R., "Gut PH, and isolation and characterization of digestive α-D-glucosidase of Sunn Pest" 12 (12): 265-274, 2010

35 Germán Bonilla-Rosso, "Functional roles and metabolic niches in the honey bee gut microbiota" Elsevier BV 43 : 69-76, 2018

36 Katie L. Mason, "From Commensal to Pathogen: Translocation of Enterococcus faecalis from the Midgut to the Hemocoel of Manduca sexta" American Society for Microbiology 2 (2): e00065-e00111, 2011

37 Anne Geiger, "First isolation of Enterobacter, Enterococcus, and Acinetobacter spp. as inhabitants of the tsetse fly (Glossina palpalis palpalis) midgut" Elsevier BV 9 (9): 1364-1370, 2009

38 Shin Yong Park, "Extracellular Gelatinase of Enterococcus faecalis Destroys a Defense System in Insect Hemolymph and Human Serum" American Society for Microbiology 75 (75): 1861-1869, 2007

39 김정명, "Effects of diet type, developmental stage, and gut compartment in the gut bacterial communities of two Cerambycidae species (Coleoptera)" 한국미생물학회 55 (55): 21-30, 2017

40 Takahiro Hosokawa, "Diversity and evolution of bacterial symbionts in the gut symbiotic organ of jewel stinkbugs (Hemiptera: Scutelleridae)" Springer Science and Business Media LLC 54 (54): 359-367, 2019

41 Scopel, W., "Culturable symbionts associated with the reproductive and digestive tissues of the Neotropical brown stinkbug Euschistus heros" 111 (111): 2413-2424, 2018

42 Yongqi Shao, "Crystallization of α- and β-carotene in the foregut of Spodoptera larvae feeding on a toxic food plant" Elsevier BV 41 (41): 273-281, 2011

43 Amiri, A., "Comparison of energy reserves in prediapause and diapausing adult Sunn pest, Eurygaster integriceps Puton(Hemiptera : Scutelleridae)" 15 : 435-444, 2013

44 Beng-Soon Teh, "Colonization of the Intestinal Tract of the Polyphagous Pest Spodoptera littoralis with the GFP-Tagged Indigenous Gut Bacterium Enterococcus mundtii" Frontiers Media SA 7 : 928-, 2016

45 Virginia Medina, "Characterized non-transient microbiota from stinkbug (Nezara viridula) midgut deactivates soybean chemical defenses" Public Library of Science (PLoS) 13 (13): e0200161-, 2018

46 Sivakumar, G., "Characterization and role of gut bacterium Bacillus pumilus on nutrition and defense of leafhopper(Amrasca biguttula biguttula)of cotton" 87 (87): 534-539, 2017

47 Bosheng Chen, "Biodiversity and Activity of the Gut Microbiota across the Life History of the Insect Herbivore Spodoptera littoralis" Springer Science and Business Media LLC 6 (6): 29505-, 2016

48 Nahomi Kaiwa, "Bacterial symbionts of the giant jewel stinkbug Eucorysses grandis (Hemiptera: Scutelleridae)" Zoological Society of Japan 28 (28): 169-174, 2011

49 Michele Souza Lima, "Bacterial community composition in the salivary glands of triatomines (Hemiptera: Reduviidae)" Public Library of Science (PLoS) 12 (12): e0006739-, 2018

50 Yu Matsuura, "Bacterial Symbionts of a Devastating Coffee Plant Pest, the Stinkbug Antestiopsis thunbergii (Hemiptera: Pentatomidae)" American Society for Microbiology 80 (80): 3769-3775, 2014

51 Hirose, E., "Bacteria in the gut of southern green stink bug(heteroptera : pentatomidae)" 99 (99): 91-95, 2006

52 Sood, P., "Bacteria associated with Bactrocera sp. (Diptera: Tephritidae)-isolation and identification" 10 : 1-9, 2002

53 Maccollom, G., "Association and attraction of blueberry maggot fly curran(Diptera : Tephritidae)to Pantoea(Enterobacter)agglomerans" 38 : 116-120, 2009

54 Schmid, R. B., "An indigenous gut bacterium, Enterococcus faecalis(Lactobacillales : Enterococcaceae), increases seed consumption by Harpalus pensylvanicus(Coleoptera : Carabidae)" 97 (97): 575-584, 2014

55 Frank Jakob, "Acetic acid bacteria encode two levansucrase types of different ecological relationship" Wiley 21 (21): 4151-4165, 2019

56 Alina S. Grigorescu, "Accessing the Hidden Microbial Diversity of Aphids: an Illustration of How Culture-Dependent Methods Can Be Used to Decipher the Insect Microbiota" Springer Science and Business Media LLC 75 (75): 1035-1048, 2018