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Abstract

Pentatomomorphan bugs can form symbiotic associations with bacteria belonging to the supergenus . This relationship has become a model for understanding environmental symbiont acquisition. Host insects can utilize various symbiont strains from across ; however, host colonization success and benefits conferred vary by bacterial clade. Therefore, we conducted a meta-analysis aimed at identifying candidate genes that underpin beneficial symbioses within this system. We scanned the entire Burkholderiaceae family for the presence of 17 colonization-associated genes, as well as 88 candidate genes that are differentially expressed during symbiosis. There was no difference in the distribution of the 17 colonization-associated genes between symbiotic ( and insect-associated plant beneficial and environmental clade) and non-symbiotic lineages; however, there was a higher prevalence of the 88 candidate genes in the insect symbiont lineages. We subsequently analysed the genomes of nine symbiotic species that confer varying fitness benefits to their insect hosts. One symbiont species was significantly worse, one was significantly better and the remaining seven were intermediate in terms of conferred host fitness benefits. We found that species possessing a higher number of the candidate genes conferred faster host development time. Furthermore, we identified two candidate genes that were missing in the least beneficial species but present in the other eight, suggesting that these genes may be important in modulating symbiont quality. Our study suggests that the mechanisms required for host colonization are broadly distributed across Burkholderiaceae, but the genes that determine symbiont quality are more prevalent in insect-associated species. This work helps to identify genes that influence this highly specialized yet diverse symbiosis between Pentatomomorphan insects and Burkholderiaceae bacteria.

Funding
This study was supported by the:
  • United States Department of Agriculture (USDA) (Award (2023-67013-39897))
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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/content/journal/mgen/10.1099/mgen.0.001333
2024-12-16
2026-03-14

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References

  1. Moran NA. Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci U S A 2007; 104:8627–8633 [View Article] [PubMed]
    [Google Scholar]
  2. Wrede C, Dreier A, Kokoschka S, Hoppert M. Archaea in symbioses. Archaea 2012; 2012:596846 [View Article] [PubMed]
    [Google Scholar]
  3. McCutcheon JP, Moran NA. Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 2012; 10:13–26 [View Article]
    [Google Scholar]
  4. Coon KL, Brown MR, Strand MR. Mosquitoes host communities of bacteria that are essential for development but vary greatly between local habitats. Mol Ecol 2016; 25:5806–5826 [View Article] [PubMed]
    [Google Scholar]
  5. Mason CJ, Couture JJ, Raffa KF. Plant-associated bacteria degrade defense chemicals and reduce their adverse effects on an insect defoliator. Oecologia 2014; 175:901–910 [View Article] [PubMed]
    [Google Scholar]
  6. Mason CJ, St Clair A, Peiffer M, Gomez E, Jones AG et al. Diet influences proliferation and stability of gut bacterial populations in herbivorous lepidopteran larvae. PLoS One 2020; 15:e0229848 [View Article] [PubMed]
    [Google Scholar]
  7. Ravenscraft A, Berry M, Hammer T, Peay K, Boggs C. Structure and function of the bacterial and fungal gut microbiota of Neotropical butterflies. Ecol Monogr 2019; 89:e01346 [View Article]
    [Google Scholar]
  8. Ravenscraft A, Kish N, Peay K, Boggs C. No evidence that gut microbiota impose a net cost on their butterfly host. Mol Ecol 2019; 28:2100–2117 [View Article] [PubMed]
    [Google Scholar]
  9. Wang Y, Eum JH, Harrison RE, Valzania L, Yang X et al. Riboflavin instability is a key factor underlying the requirement of a gut microbiota for mosquito development. Proc Natl Acad Sci U S A 2021; 118:e2101080118 [View Article] [PubMed]
    [Google Scholar]
  10. Blum WEH, Zechmeister-Boltenstern S, Keiblinger KM. Does soil contribute to the human gut microbiome?. Microorganisms 2019; 7:287 [View Article] [PubMed]
    [Google Scholar]
  11. Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T et al. Environment dominates over host genetics in shaping human gut microbiota. Nature 2018; 555:210–215 [View Article] [PubMed]
    [Google Scholar]
  12. Kikuchi Y, Hosokawa T, Fukatsu T. An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J 2011; 5:446–460 [View Article] [PubMed]
    [Google Scholar]
  13. Takeshita K, Kikuchi Y. Genomic comparison of insect gut symbionts from divergent Burkholderia subclades. Genes 2020; 11:744 [View Article] [PubMed]
    [Google Scholar]
  14. Takeshita K, Matsuura Y, Itoh H, Navarro R, Hori T et al. Burkholderia of plant-beneficial group are symbiotically associated with bordered plant bugs (Heteroptera: Pyrrhocoroidea: Largidae). Microbes Environ 2015; 30:321–329 [View Article] [PubMed]
    [Google Scholar]
  15. Acevedo TS, Fricker GP, Garcia JR, Alcaide T, Berasategui A et al. The importance of environmentally acquired bacterial symbionts for the squash bug (Anasa tristis), a significant agricultural pest. Front Microbiol 2021; 12:719112 [View Article]
    [Google Scholar]
  16. Hunter MS, Umanzor EF, Kelly SE, Whitaker SM, Ravenscraft A. Development of common leaf-footed bug pests depends on the presence and identity of their environmentally acquired symbionts. Appl Environ Microbiol 2022; 88:e0177821 [View Article] [PubMed]
    [Google Scholar]
  17. Kikuchi Y, Hosokawa T, Fukatsu T. Specific developmental window for establishment of an insect-microbe gut symbiosis. Appl Environ Microbiol 2011; 77:4075–4081 [View Article] [PubMed]
    [Google Scholar]
  18. Kikuchi Y, Hosokawa T, Fukatsu T. Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol 2007; 73:4308–4316 [View Article] [PubMed]
    [Google Scholar]
  19. Ohbayashi T, Takeshita K, Kitagawa W, Nikoh N, Koga R et al. Insect’s intestinal organ for symbiont sorting. Proc Natl Acad Sci U S A 2015; 112:E5179–E5188 [View Article] [PubMed]
    [Google Scholar]
  20. Kinosita Y, Kikuchi Y, Mikami N, Nakane D, Nishizaka T. Unforeseen swimming and gliding mode of an insect gut symbiont, Burkholderia sp. RPE64, with wrapping of the flagella around its cell body. ISME J 2018; 12:838–848 [View Article] [PubMed]
    [Google Scholar]
  21. Futahashi R, Tanaka K, Tanahashi M, Nikoh N, Kikuchi Y et al. Gene expression in gut symbiotic organ of stinkbug affected by extracellular bacterial symbiont. PLoS One 2013; 8:e64557 [View Article] [PubMed]
    [Google Scholar]
  22. Lachat J, Lextrait G, Jouan R, Boukherissa A, Yokota A et al. Hundreds of antimicrobial peptides create a selective barrier for insect gut symbionts. Microbiology 2023 [View Article]
    [Google Scholar]
  23. Jang S, Matsuura Y, Ishigami K, Mergaert P, Kikuchi Y. Symbiont coordinates stem cell proliferation, apoptosis, and morphogenesis of gut symbiotic organ in the stinkbug-Caballeronia symbiosis. Front Physiol 2022; 13:1071987 [View Article] [PubMed]
    [Google Scholar]
  24. Itoh H, Jang S, Takeshita K, Ohbayashi T, Ohnishi N et al. Host-symbiont specificity determined by microbe-microbe competition in an insect gut. Proc Natl Acad Sci U S A 2019; 116:22673–22682 [View Article] [PubMed]
    [Google Scholar]
  25. Hassen AI, Lamprecht SC, Bopape FL. Emergence of β-rhizobia as new root nodulating bacteria in legumes and current status of the legume-rhizobium host specificity dogma. World J Microbiol Biotechnol 2020; 36:40 [View Article]
    [Google Scholar]
  26. Jung M, Lee D-H. Abundance and diversity of gut-symbiotic bacteria, the genus Burkholderia in overwintering Riptortus pedestris (Hemiptera: Alydidae) populations and soil in South Korea. PLOS One 2019; 14:e0218240 [View Article] [PubMed]
    [Google Scholar]
  27. Ohbayashi T, Futahashi R, Terashima M, Barrière Q, Lamouche F et al. Comparative cytology, physiology and transcriptomics of Burkholderia insecticola in symbiosis with the bean bug Riptortus pedestris and in culture. ISME J 2019; 13:1469–1483 [View Article] [PubMed]
    [Google Scholar]
  28. Jang SH, Jang HA, Lee J, Kim JU, Lee SA et al. PhaR, a negative regulator of PhaP, modulates the colonization of a Burkholderia gut symbiont in the midgut of the host insect, Riptortus pedestris. Appl Environ Microbiol 2017; 83:e00459-17 [View Article] [PubMed]
    [Google Scholar]
  29. Jang S, Mergaert P, Ohbayashi T, Ishigami K, Shigenobu S et al. Dual oxidase enables insect gut symbiosis by mediating respiratory network formation. Proc Natl Acad Sci U S A 2021; 118:e2020922118 [View Article] [PubMed]
    [Google Scholar]
  30. Kim JK, Jang HA, Kim MS, Cho JH, Lee J et al. The lipopolysaccharide core oligosaccharide of Burkholderia plays a critical role in maintaining a proper gut symbiosis with the bean bug Riptortus pedestris. J Biol Chem 2017; 292:19226–19237 [View Article] [PubMed]
    [Google Scholar]
  31. Kim JK, Jang HA, Won YJ, Kikuchi Y, Heum Han S et al. Purine biosynthesis-deficient Burkholderia mutants are incapable of symbiotic accommodation in the stinkbug. ISME J 2014; 8:552–563 [View Article] [PubMed]
    [Google Scholar]
  32. Kim JK, Kwon JY, Kim SK, Han SH, Won YJ et al. Purine biosynthesis, biofilm formation, and persistence of an insect-microbe gut symbiosis. Appl Environ Microbiol 2014; 80:4374–4382 [View Article] [PubMed]
    [Google Scholar]
  33. Kim JK, Lee HJ, Kikuchi Y, Kitagawa W, Nikoh N et al. Bacterial cell wall synthesis gene uppP is required for Burkholderia colonization of the Stinkbug Gut. Appl Environ Microbiol 2013; 79:4879–4886 [View Article] [PubMed]
    [Google Scholar]
  34. Kim JK, Won YJ, Nikoh N, Nakayama H, Han SH et al. Polyester synthesis genes associated with stress resistance are involved in an insect-bacterium symbiosis. Proc Natl Acad Sci U S A 2013; 110:E2381–E2389 [View Article] [PubMed]
    [Google Scholar]
  35. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article] [PubMed]
    [Google Scholar]
  36. Altschul SF, Wootton JC, Gertz EM, Agarwala R, Morgulis A et al. Protein database searches using compositionally adjusted substitution matrices. FEBS J 2005; 272:5101–5109 [View Article] [PubMed]
    [Google Scholar]
  37. Stillson PT, Baltrus DA, Ravenscraft A. Prevalence of an insect-associated genomic region in environmentally acquired Burkholderiaceae symbionts. Appl Environ Microbiol 2022; 88:e0250221 [View Article] [PubMed]
    [Google Scholar]
  38. Jumper J, Evans R, Pritzel A, Green T, Figurnov M et al. Highly accurate protein structure prediction with AlphaFold. Nature 2021; 596:583–589 [View Article] [PubMed]
    [Google Scholar]
  39. Sanderson T, Bileschi ML, Belanger D, Colwell LJ. ProteInfer: deep networks for protein functional inference. Bioinformatics 2021 [View Article] [PubMed]
    [Google Scholar]
  40. Bertels F, Silander OK, Pachkov M, Rainey PB, van Nimwegen E. Automated reconstruction of whole-genome phylogenies from short-sequence reads. Mol Biol Evol 2014; 31:1077–1088 [View Article] [PubMed]
    [Google Scholar]
  41. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article] [PubMed]
    [Google Scholar]
  42. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article] [PubMed]
    [Google Scholar]
  43. Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 2019; 35:526–528 [View Article] [PubMed]
    [Google Scholar]
  44. R Core Team R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2019 https://www.R-project.org/
  45. Wiesmann CL, Wang NR, Zhang Y, Liu Z, Haney CH. Origins of symbiosis: shared mechanisms underlying microbial pathogenesis, commensalism and mutualism of plants and animals. FEMS Microbiol Rev 2023; 47:fuac048 [View Article] [PubMed]
    [Google Scholar]
  46. Hansen AK, Moran NA. Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc Natl Acad Sci U S A 2011; 108:2849–2854 [View Article] [PubMed]
    [Google Scholar]
  47. Moriyama M, Fukatsu T. Host’s demand for essential amino acids is compensated by an extracellular bacterial symbiont in a hemipteran insect model. Front Physiol 2022; 13:1028409 [View Article] [PubMed]
    [Google Scholar]
  48. Douglas AE. The B vitamin nutrition of insects: the contributions of diet, microbiome and horizontally acquired genes. Curr Opin Insect Sci 2017; 23:65–69 [View Article] [PubMed]
    [Google Scholar]
  49. Duron O, Gottlieb Y. Convergence of nutritional symbioses in obligate blood feeders. Trends Parasitol 2020; 36:816–825 [View Article] [PubMed]
    [Google Scholar]
  50. Hosokawa T, Koga R, Kikuchi Y, Meng X-Y, Fukatsu T. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci U S A 2010; 107:769–774 [View Article] [PubMed]
    [Google Scholar]
  51. Serrato-Salas J, Gendrin M. Involvement of microbiota in insect physiology: focus on B vitamins. mBio 2023; 14:e0222522 [View Article] [PubMed]
    [Google Scholar]
  52. Bellantuono AJ, Dougan KE, Granados-Cifuentes C, Rodriguez-Lanetty M. Free-living and symbiotic lifestyles of a thermotolerant coral endosymbiont display profoundly distinct transcriptomes under both stable and heat stress conditions. Mol Ecol 2019; 28:5265–5281 [View Article] [PubMed]
    [Google Scholar]
  53. Feng H, Edwards N, Anderson CMH, Althaus M, Duncan RP et al. Trading amino acids at the aphid–Buchnera symbiotic interface. Proc Natl Acad Sci USA 2019; 116:16003–16011 [View Article]
    [Google Scholar]
  54. Maltz MA, Weiss BL, O’Neill M, Wu Y, Aksoy S. OmpA-mediated biofilm formation is essential for the commensal bacterium Sodalis glossinidius to colonize the tsetse fly gut. Appl Environ Microbiol 2012; 78:7760–7768 [View Article] [PubMed]
    [Google Scholar]
  55. Roilides E, Simitsopoulou M, Katragkou A, Walsh TJ. How biofilms evade host defenses. Microbiol Spectr 2015; 3:3 [View Article] [PubMed]
    [Google Scholar]
  56. Kim JK, Kim NH, Jang HA, Kikuchi Y, Kim C-H et al. Specific midgut region controlling the symbiont population in an insect-microbe gut symbiotic association. Appl Environ Microbiol 2013; 79:7229–7233 [View Article] [PubMed]
    [Google Scholar]
  57. Park K-E, Jang SH, Lee J, Lee SA, Kikuchi Y et al. The roles of antimicrobial peptide, rip-thanatin, in the midgut of Riptortus pedestris. Develop Comparat Immunol 2018; 78:83–90 [View Article]
    [Google Scholar]
  58. Cornforth DM, Foster KR. Antibiotics and the art of bacterial war. Proc Natl Acad Sci USA 2015; 112:10827–10828 [View Article]
    [Google Scholar]
  59. Beringer JE, Brewin NJ, Johnston AWB, Schulman HM, Hopwood DA. The Rhizobium--legume symbiosis. Proc R Soc Lond B Biol Sci 1979; 204:219–233 [View Article] [PubMed]
    [Google Scholar]
  60. Jenkins BH. Mutualism on the edge: understanding the Paramecium-Chlorella symbiosis. PLOS Biol 2024; 22:e3002563 [View Article] [PubMed]
    [Google Scholar]
  61. Feldhaar H, Straka J, Krischke M, Berthold K, Stoll S et al. Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biol 2007; 5:48 [View Article] [PubMed]
    [Google Scholar]
  62. Whitehead LF, Wilkinson TL, Douglas AE. Nitrogen recycling in the pea aphid (Acyrthosiphon pisum) symbiosis. Proc R Soc Lond B 1992; 250:115–117 [View Article]
    [Google Scholar]
  63. Hu Y, Sanders JG, Łukasik P, D’Amelio CL, Millar JS et al. Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome. Nat Commun 2018; 9:964 [View Article]
    [Google Scholar]
  64. Pearson CR, Tindall SN, Potts JR, Thomas GH, Woude MW. Diverse functions for acyltransferase-3 proteins in the modification of bacterial cell surfaces: this article is part of the bacterial cell envelopes collection. Microbiology 2022; 168: [View Article]
    [Google Scholar]
  65. Pearson CR, Tindall SN, Herman R, Jenkins HT, Bateman A et al. Acetylation of surface carbohydrates in bacterial pathogens requires coordinated action of a two-domain membrane-bound acyltransferase. mBio 2020; 11:e01364-20 [View Article] [PubMed]
    [Google Scholar]
  66. Bras CP, Jordá MA, Wijfjes AHM, Harteveld M, Stuurman N et al. A Lotus japonicus nodulation system based on heterologous expression of the fucosyl transferase NodZ and the acetyl transferase NolL in Rhizobium leguminosarum. MPMI 2000; 13:475–479 [View Article]
    [Google Scholar]
  67. Davis EO, Evans IJ, Johnston AWB. Identification of nodX, a gene that allows Rhizobium leguminosarum biovar viciae strain TOM to nodulate Afghanistan peas. Mol Gen Genet 1988; 212:531–535 [View Article] [PubMed]
    [Google Scholar]
  68. Li E, Zhang H, Jiang H, Pieterse CMJ, Jousset A et al. Experimental-evolution-driven identification of Arabidopsis rhizosphere competence genes in pseudomonas protegens. mBio 2021; 12:e0092721 [View Article] [PubMed]
    [Google Scholar]
  69. Cheng H-P, Walker GC. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J Bacteriol 1998; 180:5183–5191 [View Article] [PubMed]
    [Google Scholar]
  70. Kim JK, Park HY, Lee BL. The symbiotic role of O-antigen of Burkholderia symbiont in association with host Riptortus pedestris. Develop Comparat Immunol 2016; 60:202–208 [View Article]
    [Google Scholar]
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