[en] Bacterial symbionts associated with aphids are important for their ecological fitness. The corn leaf aphid, Rhopalosiphum maidis (Fitch), is one of the most damaging aphid pests on maize and has been reported to harbor Hamiltonella defensa and Regiella insecticola while the effects of the secondary symbionts (S-symbionts) on host ecology and primary symbiont Buchnera aphidicola remain unclear. Here, four aphid strains were established, two of which were collected from Langfang - Hebei Province, China, with similar symbiont pattern except for the presence of H. defensa. Two other aphid strains were collected from Nanning - Guangxi Province, China, with the same symbiont infection except for the presence of R. insecticola. Phylogenetic analysis and aphid genotyping indicated that the S-symbiont-infected and free aphid strains from the same location had identical genetic backgrounds. Aphid fitness measurement showed that aphid strain infected with H. defensa performed shortened developmental duration for 1st instar and total nymph stages, reduced aphid survival rate, offspring, and longevity. While the developmental duration of H-infected strains was accelerated, and the adult weight was significantly higher compared to the H-free strain. Infection with R. insecticola did not affect the aphid's entire nymph stage duration and survival rate. As the H-strain does, aphids infected with R. insecticola also underwent a drop in offspring, along with marginally lower longevity. Unlike the H-infected strain, the R-infected strain performed delayed developmental duration and lower adult weight. The B. aphidicola titers of the H-infected strains showed a steep drop during the aphid 1st to 3rd instar stages, while the augmentation of B. aphidicola titers was found in the R-infected strain during the aphid 1st to 3rd instar. Our study investigated for the first time the effect of the S-symbionts on the ecology fitness and primary symbiont in R. maidis, indicating that infection with secondary symbionts leads to the modulation of aphid primary symbiont abundance, together inducing significant fitness costs on aphids with further impact on environmental adaptation and trophic interactions.
Disciplines :
Entomology & pest control
Author, co-author :
Liu, Shen ; Université de Liège - ULiège > Gembloux Agro-Bio Tech > Gembloux Agro-Bio Tech ; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Liu, Xiaobei ; Université de Liège - ULiège > Gembloux Agro-Bio Tech > Form. doct. sc. agro. & ingé. biol. (paysage) ; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Zhang, Tiantao; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Bai, Shuxiong; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
He, Kanglai; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Zhang, Yongjun; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Francis, Frédéric ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs
Wang, Zhenying; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Language :
English
Title :
Secondary symbionts affect aphid fitness and the titer of primary symbiont.
SL, FF, and ZW conceptualized the study. TZ, SB, KH, and YZ assisted in the experimental methods. SL performed the experiment, XL assisted in the experiment of aphid fitness measurement. SL wrote the manuscript. FF and ZW reviewed and amended the manuscript. ZW provided financial support. All authors contributed to the article and approved the submitted version.
Burke G. Fiehn O. Moran N. A. (2010). Effects of facultative symbionts and heat stress on the metabolome of pea aphids. ISME. J. 4, 242–252. doi: 10.1038/ismej.2009.114
Cayetano L. Rothacher L. Simon J. C. Vorburger C. (2015). Cheaper is not always worse: strongly protective isolates of a defensive symbiont are less costly to the aphid host. Proc. Biol. Sci. 282, 20142333. doi: 10.1098/rspb.2014.2333
Chen Y. Quan Y. Verheggen F. Wang Z. Francis F. He K. (2020). Differential thermal tolerance across life stages under extreme high temperatures crossed with feeding status in corn leaf aphid. Ecol. Entomol. 46, 533–540. doi: 10.1111/een.12998
Chen W. Shakir S. Bigham M. Richter A. Fei Z. Jander G. (2019). Genome sequence of the corn leaf aphid (Rhopalosiphum maidis Fitch). Gigascience 8, giz033. doi: 10.1093/gigascience/giz033
Chong R. A. Park H. Moran N. A. (2019). Genome evolution of the obligate endosymbiont Buchnera aphidicola. Mol. Biol. Evol. 36, 1481–1489. doi: 10.1093/molbev/msz082
Csorba A. B. Fora C. G. Bálint J. Felföldi T. Szabó A. Máthé I. et al. (2022). Endosymbiotic bacterial diversity of corn leaf aphid, Rhopalosiphum maidis Fitch (Hemiptera: Aphididae) associated with maize management systems. Microorganisms 10, 939. doi: 10.3390/microorganisms10050939
De Clerck C. Fujiwara A. Joncour P. Léonard S. Félix M. L. Francis F. et al. (2015). A metagenomic approach from aphid’s hemolymph sheds light on the potential roles of co-existing endosymbionts. Microbiome 3, 63. doi: 10.1186/s40168-015-0130-5
Douglas A. E. (2015). Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60, 17–34. doi: 10.1146/annurev-ento-010814-020822
Fakhour S. Ambroise J. Renoz F. Foray V. Gala J. L. Hance T. (2018). A large-scale field study of bacterial communities in cereal aphid populations across Morocco. FEMS. Microbiol. Ecol. 94, fiy003. doi: 10.1093/femsec/fiy003
Guidolin A. S. Cônsoli F. L. (2017). Symbiont diversity of aphis (Toxoptera) citricidus (Hemiptera: Aphididae) as influenced by host plants. Microb. Ecol. 73, 201–210. doi: 10.1007/s00248-016-0892-8
Guo J. Liu X. Poncelet N. He K. Francis F. Wang Z. (2019). Detection and geographic distribution of seven facultative endosymbionts in two Rhopalosiphum aphid species. MicrobiologyOpen 8, e00817. doi: 10.1002/mbo3.817
Henry L. M. Maiden M. C. Ferrari J. Godfray H. C. (2015). Insect life history and the evolution of bacterial mutualism. Ecol. Lett. 18, 516–525. doi: 10.1111/ele.12425
Herren J. K. Lemaitre B. (2011). Spiroplasma and host immunity: activation of humoral immune responses increases endosymbiont load and susceptibility to certain gram-negative bacterial pathogens in Drosophila melanogaster. Cell Microbiol. 13, 1385–1396. doi: 10.1111/j.1462-5822.2011.01627.x
Karley A. J. Emslie-Smith M. Bennett A. E. (2017). Potato aphid Macrosiphum euphorbiae performance is determined by aphid genotype and not mycorrhizal fungi or water availability. Insect Sci. 24, 1015–1024. doi: 10.1111/1744-7917.12445
Koga R. Tsuchida T. Fukatsu T. (2003). Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc. Biol. Sci. 270, 2543–2550. doi: 10.1098/rspb.2003.2537
Kumar S. Tamura K. Jakobsen I. B. Nei M. (2001). MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245. doi: 10.1093/bioinformatics/17.12.1244
Laughton A. M. Fan M. H. Gerardo N. M. (2014). The combined effects of bacterial symbionts and aging on life history traits in the pea aphid, Acyrthosiphon pisum. Appl. Environ. Microbiol. 80, 470–477. doi: 10.1128/AEM.02657-13
Leclair M. Polin S. Jousseaume T. Simon J. C. Sugio A. Morlière S. et al. (2017). Consequences of coinfection with protective symbionts on the host phenotype and symbiont titres in the pea aphid system. Insect Sci. 24, 798–808. doi: 10.1111/1744-7917.12380
Leybourne D. J. Bos J. I. B. Valentine T. A. Karley A. J. (2020a). The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry-oat aphid, Rhopalosiphum padi. Insect Sci. 27, 69–85. doi: 10.1111/1744-7917.12606
Leybourne D. J. Melloh P. Martin E. A. (2022). Common facultative endosymbionts do not influence sensitivity of cereal aphids to pyrethroids. Agr. Forest. Entomol., 25, 1–11. doi: 10.1111/afe.12539
Leybourne D. J. Valentine T. A. Bos J. I. B. Karley A. J. (2020b). A fitness cost resulting from hamiltonella defensa infection is associated with altered probing and feeding behaviour in Rhopalosiphum padi. J. Exp. Biol. 223, jeb207936. doi: 10.1242/jeb.207936
Li Q. Fan J. Sun J. Wang M. Chen J. (2018). Effect of the secondary symbiont Hamiltonella defensa on fitness and relative abundance of Buchnera aphidicola of wheat aphid, Sitobion miscanthi. Front. Microbiol. 9. doi: 10.3389/fmicb.2018.00582
Li Q. Fan J. Sun J. Zhang Y. Hou M. Chen J. (2019). Anti-plant defense response strategies mediated by the secondary symbiont Hamiltonella defensa in the wheat aphid Sitobion miscanthi. Front. Microbiol. 10. doi: 10.3389/fmicb.2019.02419
Li Q. Sun J. Qin Y. Fan J. Zhang Y. Tan X. et al. (2021). Reduced insecticide susceptibility of the wheat aphid Sitobion miscanthi after infection by the secondary bacterial symbiont Hamiltonella defensa. Pest Manage. Sci. 77, 1936–1944. doi: 10.1002/ps.6221
Liu X. Lei H. Chen F. (2019). Infection pattern and negative effects of a facultative endosymbiont on its insect host are environment-dependent. Sci. Rep. 9, 4013. doi: 10.1038/s41598-019-40607-5
Łukasik P. Dawid M. A. Ferrari J. Godfray H. C. (2013). The diversity and fitness effects of infection with facultative endosymbionts in the grain aphid, Sitobion avenae. Oecologia 173, 985–996. doi: 10.1007/s00442-013-2660-5
Luo C. Gatti J.-L. Monticelli L. S. Poirié Marylène. Desneux N. Zhao H. et al. (2020a). An increased risk of parasitism mediated by the facultative symbiont Regiella insecticola. J. Pest Sci. 93, 737–745. doi: 10.1007/s10340-019-01189-3
Luo C. Monticelli L. S. Li D. Ahmed S. S. Pandharikar G. G. Zhao H. et al. (2020b). Comparison of life-history traits and resistance for Sitobion avenae (Fabricius) harboring a facultative symbiont. Entomol. Gen. 40, 39–47. doi: 10.1127/entomologia/2019/0823
Martinez A. J. Weldon S. R. Oliver K. M. (2014). Effects of parasitism on aphid nutritional and protective symbioses. Mol. Ecol. 23, 1594–1607. doi: 10.1111/mec.12550
Mathé-Hubert H. Kaech H. Ganesanandamoorthy P. Vorburger C. (2019). Evolutionary costs and benefits of infection with diverse strains of Spiroplasma in pea aphids. Evolution 73, 1466–1481. doi: 10.1111/evo.13740
McLean A. H. Godfray H. C. (2015). Evidence for specificity in symbiont-conferred protection against parasitoids. Proc. Biol. Sci. 282, 20150977. doi: 10.1098/rspb.2015.0977
Meseguer A. S. Manzano-Marín A. Coeur d’Acier A. Clamens A.-L. Godefroid M. Jousselin E. (2017). Buchnera has changed flatmate but the repeated replacement of co-obligate symbionts is not associated with the ecological expansions of their aphid hosts. Mol. Ecol. 26, 2363–2378. doi: 10.1111/mec.13910
Montllor C. B. Maxmen A. Purcell A. H. (2002). Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol. Entomol. 27, 189–195. doi: 10.1046/j.1365-2311.2002.00393.x
Moran N. A. McCutcheon J. P. Nakabachi A. (2008). Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42, 165–190. doi: 10.1146/annurev.genet.41.110306.130119
Mouton L. Henri H. Charif D. Boulétreau M. Vavre F. (2007). Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Biol. Lett. 3, 210–213. doi: 10.1098/rsbl.2006.0590
Myint Y. Y. Bai S. Zhang T. Babendreier D. He K. Wang Z. (2021). Molecular and morphological identification of Trichogramma (Hymenoptera: Trichogrammatidae) species from Asian corn borer (Lepidoptera: Crambidae) in Myanmar. J. Econ. Entomol. 114, 40–49. doi: 10.1093/jee/toaa253
Neiers F. Saliou J. M. Briand L. Robichon A. (2021). Adaptive variation of Buchnera endosymbiont density in aphid host Acyrthosiphon pisum controlled by environmental conditions. ACS Omega 6, 17902–17914. doi: 10.1021/acsomega.1c01465
Oliver K. M. Higashi C. H. (2019). Variations on a protective theme: Hamiltonella defensa infections in aphids variably impact parasitoid success. Curr. Opin. Insect Sci. 32, 1–7. doi: 10.1016/j.cois.2018.08.009
Oliver K. M. Smith A. H. Russell J. A. (2014). Defensive symbiosis in the real world - advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct. Ecol. 28, 341–355. doi: 10.1111/1365-2435.12133
Parker B. J. Spragg C. J. Altincicek B. Gerardo N. M. (2013). Symbiont-mediated protection against fungal pathogens in pea aphids: a role for pathogen specificity? Appl. Environ. Microbiol. 79, 2455–2458. doi: 10.1128/AEM.03193-12
Patel V. Chevignon G. Manzano-Marín A. Brandt J. W. Strand M. R. Russell J. A. et al. (2019). Cultivation-assisted genome of candidatus Fukatsuia symbiotica; the enigmatic “X-type”symbiont aphids. Genome Biol. Evol. 11, 3510–3522. doi: 10.1093/gbe/evz252
Perreau J. Zhang B. Maeda G. P. Kirkpatrick M. Moran N. A. (2021). Strong within-host selection in a maternally inherited obligate symbiont: Buchnera and aphids. Proc. Natl. Acad. Sci. U S A 118, e2102467118. doi: 10.1073/pnas.2102467118
Pons I. Scieur N. Dhondt L. Renard M. E. Renoz F. Hance T. (2022). Pervasiveness of the symbiont Serratia symbiotica in the aphid natural environment: distribution, diversity and evolution at a multitrophic level. FEMS. Microbiol. Ecol. 98, 1–15. doi: 10.1093/femsec/fiac012
Scarborough C. L. Ferrari J. Godfray H. C. (2005). Aphid protected from pathogen by endosymbiont. Science 310, 1781. doi: 10.1126/science.1120180
Shigenobu S. Watanabe H. Hattori M. Sakaki Y. Ishikawa H. (2000). Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407, 81–86. doi: 10.1038/35024074
Simon J. C. Boutin S. Tsuchida T. Koga R. Le Gallic J. F. Frantz A. et al. (2011). Facultative symbiont infections affect aphid reproduction. PLoS One 6, e21831. doi: 10.1371/journal.pone.0021831
Simonet P. Duport G. Gaget K. Weiss-Gayet M. Colella S. Febvay G. et al. (2016). Direct flow cytometry measurements reveal a fine-tuning of symbiotic cell dynamics according to the host developmental needs in aphid symbiosis. Sci. Rep. 6, 19967. doi: 10.1038/srep19967
Skaljac M. Kirfel P. Grotmann J. Vilcinskas A. (2018). Fitness costs of infection with Serratia symbiotica are associated with greater susceptibility to insecticides in the pea aphid Acyrthosiphon pisum. Pest Manage. Sci. 74, 1829–1836. doi: 10.1002/ps.4881
Tsuchida T. Koga R. Horikawa M. Tsunoda T. Maoka T. Matsumoto S. et al. (2010). Symbiotic bacterium modifies aphid body color. Science 330, 1102–1104. doi: 10.1126/science.1195463
Vogel K. J. Moran N. A. (2011). Effect of host genotype on symbiont titer in the aphid-Buchnera symbiosis. Insects 2, 423–434. doi: 10.3390/insects2030423
Vorburger C. Gehrer L. Rodriguez P. (2010). A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biol. Lett. 6, 109–111. doi: 10.1098/rsbl.2009.0642
Vorburger C. Rouchet R. (2016). Are aphid parasitoids locally adapted to the prevalence of defensive symbionts in their hosts? BMC Evol. Biol. 16, 271. doi: 10.1186/s12862-016-0811-0
Wang D. Shi X. Dai P. Liu D. Dai X. Shang Z. et al. (2016). Comparison of fitness traits and their plasticity on multiple plants for Sitobion avenae infected and cured of a secondary endosymbiont. Sci. Rep. 6, 23177. doi: 10.1038/srep23177
Whelan J. A. Russell N. B. Whelan M. A. (2003). A method for the absolute quantification of cDNA using real-time PCR. J. Immunol. Methods 278, 261–269. doi: 10.1016/s0022-1759(03)00223-0
Wilkinson T. L. Adams D. Minto L. B. Douglas A. E. (2001). The impact of host plant on the abundance and function of symbiotic bacteria in an aphid. J. Exp. Biol. 204, 3027–3038. doi: 10.1242/jeb.204.17.3027
Wilson A. C. C. Massonnet B. Simon J. C. Prunier-Leterme N. Dolatti L. Llewellyn K. S. et al. (2004). Cross-species amplification of microsatellite loci in aphids: assessment and application. Mol. Ecol. Notes 4, 104–109. doi: 10.1046/j.1471-8286.2004.00584.x
Wu T. P. Monnin D. Lee R. A. R. Henry L. M. (2022). Local adaptation to hosts and parasitoids shape Hamiltonella defensa genotypes across aphid species. Proc. Biol. Sci. 289, 20221269. doi: 10.1098/rspb.2022.1269
Zhang B. Leonard S. P. Li Y. Moran. N. A. (2019). Obligate bacterial endosymbionts limit thermal tolerance of insect host species. Proc. Natl. Acad. Sci. U S A 116, 24712–24718. doi: 10.1073/pnas.1915307116
Zhang Y. Cao W. Zhong L. Godfray H. C. J. Liu X. (2016). Host plant determines the population size of an obligate symbiont (Buchnera aphidicola) in aphids. Appl. Environ. Microbiol. 82, 2336–46. doi: 10.1128/AEM.04131-15
Zytynska S. E. Tighiouart K. Frago E. (2021). Benefits and costs of hosting facultative symbionts in plant-sucking insects: A meta-analysis. Mol. Ecol. 30, 2483–2494. doi: 10.1111/mec.15897