Hostname: page-component-848d4c4894-ttngx Total loading time: 0 Render date: 2024-05-07T18:02:49.830Z Has data issue: false hasContentIssue false
  • English
  • Français

Composition and diversity of the gut microbiota across different life stages of American cockroach (Periplaneta americana)

Published online by Cambridge University Press:  01 December 2023

Zhiyu Chen Open the ORCID record for Zhiyu Chen [Opens in a new window] ,
Sihao Wen ,
Juan Shen ,
Jie Wang ,
Wenbin Liu Open the ORCID record for Wenbin Liu [Opens in a new window]  and
Xiaobao Jin Open the ORCID record for Xiaobao Jin [Opens in a new window]
Zhiyu Chen
Affiliation:
Guangdong Provincial Key Laboratory of Pharmaceutical Bioactive Substances, Guangdong Pharmaceutical University, Guangzhou, Guangdong 510006, PR China School of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou, Guangdong 510006, PR China
Sihao Wen
Affiliation:
Guangdong Provincial Key Laboratory of Pharmaceutical Bioactive Substances, Guangdong Pharmaceutical University, Guangzhou, Guangdong 510006, PR China School of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou, Guangdong 510006, PR China
Juan Shen
Affiliation:
Guangdong Provincial Key Laboratory of Pharmaceutical Bioactive Substances, Guangdong Pharmaceutical University, Guangzhou, Guangdong 510006, PR China School of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou, Guangdong 510006, PR China
Jie Wang
Affiliation:
Guangdong Provincial Key Laboratory of Pharmaceutical Bioactive Substances, Guangdong Pharmaceutical University, Guangzhou, Guangdong 510006, PR China School of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou, Guangdong 510006, PR China
Wenbin Liu*
Affiliation:
Guangdong Provincial Key Laboratory of Pharmaceutical Bioactive Substances, Guangdong Pharmaceutical University, Guangzhou, Guangdong 510006, PR China School of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou, Guangdong 510006, PR China
Xiaobao Jin*
Affiliation:
Guangdong Provincial Key Laboratory of Pharmaceutical Bioactive Substances, Guangdong Pharmaceutical University, Guangzhou, Guangdong 510006, PR China School of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou, Guangdong 510006, PR China
*
Corresponding authors: Wenbin Liu; Email: 408011126@qq.com; Xiaobao Jin; Email: jinxf2001@163.com
Corresponding authors: Wenbin Liu; Email: 408011126@qq.com; Xiaobao Jin; Email: jinxf2001@163.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Periplaneta americana, one of the most widely distributed insects all over the world, can survive and reproduce in harsh environment which may be closely related to the critical roles of intestinal microorganisms in its multiple physiological functions. However, the composition and structure of gut microbiota throughout different life stages and its effects on the strong resilient and environmental adaptability of P. americana remain unclear. In this study, the gut microbiota across life stages including ootheca (embryos), nymph and adult of P. americana were investigated by 16S rRNA high-throughput sequencing. Multivariate statistical analysis showed the richness and diversity of bacterial communities were significantly different among ootheca, nymph and adult stage of P. americana. Taxonomic analysis showed Blattabacterium was the dominant genus in bacterial community of ootheca while the nutrient absorption-related genera including Christensenellaceae and Ruminococcaceae showed high relative abundance in nymph samples. Moreover, functional prediction analysis showed the metabolic categories in ootheca might have more influence on the basic life activities of the host than improved production and viability, while it was more associated to the society activities, reproduction and development of host in nymph and adult. It was suggested that the gut microbiota in each life stage might meet the requirements for environmental adaptability and survival of P. americana via transforming the composition and structure with specific metabolic capabilities. Overall, these results provided a novel sight to better understand the strong vitality and adaptability throughout life stages of P. americana.

Keywords

gut microbiotalife cyclePeriplaneta americana16S rRNA high-throughput sequencing
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 113 , Issue 6 , December 2023 , pp. 787 - 793
Check for updates
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

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.)

Footnotes

*

These authors contributed equally to this work.

References

Agus, A, Clément, K and Sokol, H (2021) Gut microbiota-derived metabolites as central regulators in metabolic disorders. Gut 70, 1174–1182.CrossRefGoogle ScholarPubMed
Aharon, Y, Pasternak, Z, Ben Yosef, M, Behar, A, Lauzon, C, Yuval, B and Jurkevitch, E (2013) Phylogenetic, metabolic, and taxonomic diversities shape Mediterranean fruit fly microbiotas during ontogeny. Applied and Environmental Microbiology 79, 303–313.CrossRefGoogle ScholarPubMed
Arya, H, Toltesi, R, Eng, M, Garg, D, Merritt, TJS and Rajpurohit, S (2021) No water, no mating: connecting dots from behaviour to pathways. PLoS ONE 16, e0252920.CrossRefGoogle ScholarPubMed
Ayayee, PA, Ondrejech, A, Keeney, G and Muñoz-Garcia, A (2018) The role of gut microbiota in the regulation of standard metabolic rate in female Periplaneta americana. PeerJ 6, e4717.CrossRefGoogle ScholarPubMed
Berlanga, M (2015) Functional symbiosis and communication in microbial ecosystems. The case of wood-eating termites and cockroaches. International Microbiology 18, 159–169.Google ScholarPubMed
Bertino-Grimaldi, D, Medeiros, MN, Vieira, RP, Cardoso, AM, Turque, AS, Silveira, CB, Albano, RM, Bressan-Nascimento, S, Garcia, ES, de Souza, W, Martins, OB and Machado, EA (2013) Bacterial community composition shifts in the gut of Periplaneta americana fed on different lignocellulosic materials. SpringerPlus 2, 609.CrossRefGoogle ScholarPubMed
Bokulich, NA, Subramanian, S, Faith, JJ, Gevers, D, Gordon, JI, Knight, R, Mills, DA and Caporaso, JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nature Methods 10, 57–59.CrossRefGoogle ScholarPubMed
Cani, PD, Van Hul, M, Lefort, C, Depommier, C, Rastelli, M and Everard, A (2019) Microbial regulation of organismal energy homeostasis. Nature Metabolism 1, 34–46.CrossRefGoogle ScholarPubMed
Caporaso, JG, Kuczynski, J, Stombaugh, J, Bittinger, K, Bushman, FD, Costello, EK, Fierer, N, Peña, AG, Goodrich, JK, Gordon, JI, Huttley, GA, Kelley, ST, Knights, D, Koenig, JE, Ley, RE, Lozupone, CA, McDonald, D, Muegge, BD, Pirrung, M, Reeder, J, Sevinsky, JR, Turnbaugh, PJ, Walters, WA, Widmann, J, Yatsunenko, T, Zaneveld, J and Knight, R (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336.CrossRefGoogle ScholarPubMed
Cheng, D, Guo, Z, Riegler, M, Xi, Z, Liang, G and Xu, Y (2017) Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel). Microbiome 5, 13.CrossRefGoogle Scholar
Chouaia, B, Goda, N, Mazza, G, Alali, S, Florian, F, Gionechetti, F, Callegari, M, Gonella, E, Magoga, G, Fusi, M, Crotti, E, Daffonchio, D, Alma, A, Paoli, F, Roversi, PF, Marianelli, L and Montagna, M (2019) Developmental stages and gut microenvironments influence gut microbiota dynamics in the invasive beetle Popillia japonica Newman (Coleoptera: Scarabaeidae). Environmental Microbiology 21, 4343–4359.CrossRefGoogle Scholar
Edgar, RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.CrossRefGoogle ScholarPubMed
Estes, AM, Hearn, DJ, Snell-Rood, EC, Feindler, M, Feeser, K, Abebe, T, Dunning Hotopp, JC and Moczek, AP (2013) Brood ball-mediated transmission of microbiome members in the dung beetle, Onthophagus taurus (Coleoptera: Scarabaeidae). PLoS ONE 8, e79061.CrossRefGoogle Scholar
Feldhaar, H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecological Entomology 36, 533–543.CrossRefGoogle Scholar
Flint, HJ, Scott, KP, Duncan, SH, Louis, P and Forano, E (2012) Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3, 289–306.CrossRefGoogle ScholarPubMed
Guzman, J and Vilcinskas, A (2020) Bacteria associated with cockroaches: health risk or biotechnological opportunity? Applied Microbiology and Biotechnology 104, 10369–10387.CrossRefGoogle ScholarPubMed
Heermann, R and Fuchs, TM (2008) Comparative analysis of the Photorhabdus luminescens and the Yersinia enterocolitica genomes: uncovering candidate genes involved in insect pathogenicity. BMC Genomics 9, 40.CrossRefGoogle ScholarPubMed
Jahnes, BC, Herrmann, M and Sabree, ZL (2019) Conspecific coprophagy stimulates normal development in a germ-free model invertebrate. PeerJ 7, e6914.CrossRefGoogle Scholar
Lee, S, Kim, JY, Yi, M-H, Lee, I-Y, Lee, W-J, Moon, HS, Yong, D and Yong, T-S (2020) Comparative microbiome analysis of three species of laboratory-reared periplaneta cockroaches. The Korean Journal of Parasitology 58, 537–542.CrossRefGoogle ScholarPubMed
Liu, N, Zhang, L, Zhou, H, Zhang, M, Yan, X, Wang, Q, Long, Y, Xie, L, Wang, S, Huang, Y and Zhou, Z (2013) Metagenomic insights into metabolic capacities of the gut microbiota in a fungus-cultivating termite (Odontotermes yunnanensis). PLoS ONE 8, e69184.CrossRefGoogle Scholar
Magoč, T and Salzberg, SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963.CrossRefGoogle ScholarPubMed
Malacrinò, A, Campolo, O, Medina, RF and Palmeri, V (2018) Instar- and host-associated differentiation of bacterial communities in the Mediterranean fruit fly Ceratitis capitata. PLoS ONE 13, e0194131.CrossRefGoogle ScholarPubMed
Nicholson, JK, Holmes, E, Kinross, J, Burcelin, R, Gibson, G, Jia, W and Pettersson, S (2012) Host-gut microbiota metabolic interactions. Science 336, 1262–1267.CrossRefGoogle ScholarPubMed
Noma, T (2005) Dynamics of nucleotide metabolism as a supporter of life phenomena. The Journal of Medical Investigation: JMI 52, 127–136.CrossRefGoogle ScholarPubMed
Rodrigues, JLM, Pellizari, VH, Mueller, R, Baek, K, Jesus, EdC, Paula, FS, Mirza, B, Hamaoui, GS, Tsai, SM, Feigl, B, Tiedje, JM, Bohannan, BJM and Nüsslein, K (2013) Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proceedings of the National Academy of Sciences of the USA 110, 988–993.CrossRefGoogle ScholarPubMed
Sabree, ZL, Kambhampati, S and Moran, NA (2009) Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proceedings of the National Academy of Sciences of the USA 106, 19521–19526.CrossRefGoogle ScholarPubMed
Schwab, DB, Riggs, HE, Newton, ILG and Moczek, AP (2016) Developmental and ecological benefits of the maternally transmitted microbiota in a dung beetle. The American Naturalist 188, 679–692.CrossRefGoogle Scholar
Stock, AM, Robinson, VL and Goudreau, PN (2000) Two-component signal transduction. Annual Review of Biochemistry 69, 183–215.CrossRefGoogle ScholarPubMed
Taylor, RL and Freckleton, WC (1969) Sex differences in longevity of starved cockroaches (Leucophaea maderae). Journal of Invertebrate Pathology 13, 68–73.CrossRefGoogle ScholarPubMed
Vacchini, V, Gonella, E, Crotti, E, Prosdocimi, EM, Mazzetto, F, Chouaia, B, Callegari, M, Mapelli, F, Mandrioli, M, Alma, A and Daffonchio, D (2017) Bacterial diversity shift determined by different diets in the gut of the spotted wing fly Drosophila suzukii is primarily reflected on acetic acid bacteria. Environmental Microbiology Reports 9, 91–103. https://doi.org/10.1111/1758-2229.12505CrossRefGoogle ScholarPubMed
Vera-Ponce de León, A, Jahnes, BC, Duan, J, Camuy-Vélez, LA and Sabree, ZL (2020) Cultivable, host-specific bacteroidetes symbionts exhibit diverse polysaccharolytic strategies. Applied and Environmental Microbiology 86, e00091-20. https://doi.org/10.1128/AEM.00091-20CrossRefGoogle ScholarPubMed
Walters, W, Hyde, ER, Berg-Lyons, D, Ackermann, G, Humphrey, G, Parada, A, Gilbert, JA, Jansson, JK, Caporaso, JG, Fuhrman, JA, Apprill, A and Knight, R (2016) Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. MSystems 1, 00009-15.CrossRefGoogle ScholarPubMed
Wharton, ML and Wharton, DRA (1957) The production of sex attractant substance and of oothecae by the normal and irradiated American cockroach, Periplaneta americana L. Journal of Insect Physiology 1, 229–239.CrossRefGoogle Scholar
Yu, Y, Lee, C, Kim, J and Hwang, S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnology and Bioengineering 89, 670–679.CrossRefGoogle ScholarPubMed
Zhang, J, Blessing, D, Wu, C, Liu, N, Li, J, Qin, S and Li, M (2017) Comparative transcriptomes analysis of the wing disc between two silkworm strains with different size of wings. PLoS ONE 12, e0179560.CrossRefGoogle ScholarPubMed
Zhang, J-H, Zhang, S, Yang, Y-X, Zhang, Y-X and Liu, Z-W (2018) New insight into foregut functions of xenobiotic detoxification in the cockroach Periplaneta americana. Insect Science 25, 978–990.CrossRefGoogle ScholarPubMed
Zhukova, M, Sapountzis, P, Schiøtt, M and Boomsma, JJ (2017) Diversity and transmission of gut bacteria in Atta and Acromyrmex leaf-cutting ants during development. Frontiers in Microbiology 8, 1942.CrossRefGoogle ScholarPubMed
Supplementary material: File

Chen et al. supplementary material

Chen et al. supplementary material
Download Chen et al. supplementary material(File)
File 775.8 KB