The Links Between Dietary Diversity and RNA Virus Diversity Harbored by the Great Evening Bat (Ia Io)

Overview

Journal Microbiome

Publisher Biomed Central

Specialties Genetics
Microbiology

Date 2024 Nov 23

PMID 39578858

Authors

Zhenglanyi Huang

Zhiqiang Wang

Yingying Liu

Can Ke

Jiang Feng

Biao He

Tinglei Jiang

Affiliations

Soon will be listed here.

Abstract

Background: Predator‒prey interactions and their dynamic changes provide frequent opportunities for viruses to spread among organisms and thus affect their virus diversity. However, the connections between dietary diversity and virus diversity in predators have seldom been studied. The avivorous bats, Ia io, show a seasonal pattern of dietary diversity. Although most of them primarily prey on insects in summer, they mainly prey on nocturnally migrating birds in spring and autumn.

Results: In this study, we characterized the RNA virome of three populations of I. io in Southwest China during summer and autumn using viral metatranscriptomic sequencing. We also investigated the relationships between dietary diversity and RNA virus diversity by integrating DNA metabarcoding and viral metatranscriptomic sequencing techniques at the population level of I. io. We found 55 known genera belonging to 35 known families of RNA viruses. Besides detecting mammal-related viruses, which are the usual concern, we also found a high abundance of insect-related viruses and some bird-related viruses. We found that insect-related viruses were more abundant in summer, while the bird-related viruses were predominantly detected in autumn, which might be caused by the seasonal differences in prey selection by I. io. Additionally, a significant positive correlation was identified between prey diversity and total virus diversity. The more similar the prey composition, the more similar the total virus composition and the higher the count of potential new viruses. We also found that the relative abundance of Picornaviridae increased with increasing prey diversity and body mass.

Conclusions: In this study, significant links were found between RNA virus diversity and dietary diversity of I. io. The results implied that dynamic changes in predator-prey interactions may facilitate frequent opportunities for viruses to spread among organisms. Video Abstract.

References

Sun Y, Qu Y, Yan X, Yan G, Chen J, Wang G . Comprehensive Evaluation of RNA and DNA Viromic Methods Based on Species Richness and Abundance Analyses Using Marmot Rectal Samples. mSystems. 2022; 7(4):e0043022. PMC: 9426427. DOI: 10.1128/msystems.00430-22. View

Gong L, Geng Y, Wang Z, Lin A, Wu H, Feng L . Behavioral innovation and genomic novelty are associated with the exploitation of a challenging dietary opportunity by an avivorous bat. iScience. 2022; 25(9):104973. PMC: 9459691. DOI: 10.1016/j.isci.2022.104973. View

French R, Holmes E . An Ecosystems Perspective on Virus Evolution and Emergence. Trends Microbiol. 2019; 28(3):165-175. DOI: 10.1016/j.tim.2019.10.010. View

Langmead B, Salzberg S . Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012; 9(4):357-9. PMC: 3322381. DOI: 10.1038/nmeth.1923. View

Papkou A, Guzella T, Yang W, Koepper S, Pees B, Schalkowski R . The genomic basis of Red Queen dynamics during rapid reciprocal host-pathogen coevolution. Proc Natl Acad Sci U S A. 2019; 116(3):923-928. PMC: 6338873. DOI: 10.1073/pnas.1810402116. View

Tong S, Li Y, Rivailler P, Conrardy C, Alvarez Castillo D, Chen L . A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci U S A. 2012; 109(11):4269-74. PMC: 3306675. DOI: 10.1073/pnas.1116200109. View

Guy C, Thiagavel J, Mideo N, Ratcliffe J . Phylogeny matters: revisiting 'a comparison of bats and rodents as reservoirs of zoonotic viruses'. R Soc Open Sci. 2019; 6(2):181182. PMC: 6408376. DOI: 10.1098/rsos.181182. View

Speakman J . Body size, energy metabolism and lifespan. J Exp Biol. 2005; 208(Pt 9):1717-30. DOI: 10.1242/jeb.01556. View

Huang Z, de Boer W, van Langevelde F, Olson V, Blackburn T, Prins H . Species' life-history traits explain interspecific variation in reservoir competence: a possible mechanism underlying the dilution effect. PLoS One. 2013; 8(1):e54341. PMC: 3554779. DOI: 10.1371/journal.pone.0054341. View

10.

Kraberger S, Fountain-Jones N, Gagne R, Malmberg J, Dannemiller N, Logan K . Frequent cross-species transmissions of foamy virus between domestic and wild felids. Virus Evol. 2020; 6(1):vez058. PMC: 6955097. DOI: 10.1093/ve/vez058. View

11.

Mollentze N, Streicker D . Viral zoonotic risk is homogenous among taxonomic orders of mammalian and avian reservoir hosts. Proc Natl Acad Sci U S A. 2020; 117(17):9423-9430. PMC: 7196766. DOI: 10.1073/pnas.1919176117. View

12.

Luis A, Hayman D, OShea T, Cryan P, Gilbert A, Pulliam J . A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special?. Proc Biol Sci. 2013; 280(1756):20122753. PMC: 3574368. DOI: 10.1098/rspb.2012.2753. View

13.

Jones K, Patel N, Levy M, Storeygard A, Balk D, Gittleman J . Global trends in emerging infectious diseases. Nature. 2008; 451(7181):990-3. PMC: 5960580. DOI: 10.1038/nature06536. View

14.

Chen Y, Hu S, Lin X, Tian J, Lv J, Wang M . Host traits shape virome composition and virus transmission in wild small mammals. Cell. 2023; 186(21):4662-4675.e12. DOI: 10.1016/j.cell.2023.08.029. View

15.

Ibanez C, Juste J . Bat predation on nocturnally migrating birds. Proc Natl Acad Sci U S A. 2001; 98(17):9700-2. PMC: 55515. DOI: 10.1073/pnas.171140598. View

16.

Schoch C, Ciufo S, Domrachev M, Hotton C, Kannan S, Khovanskaya R . NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database (Oxford). 2020; 2020. PMC: 7408187. DOI: 10.1093/database/baaa062. View

17.

Turmelle A, Olival K . Correlates of viral richness in bats (order Chiroptera). Ecohealth. 2010; 6(4):522-39. PMC: 7088156. DOI: 10.1007/s10393-009-0263-8. View

18.

Gong L, Shi B, Wu H, Feng J, Jiang T . Who's for dinner? Bird prey diversity and choice in the great evening bat, . Ecol Evol. 2021; 11(13):8400-8409. PMC: 8258197. DOI: 10.1002/ece3.7667. View

19.

Wang J, Pan Y, Yang L, Yang W, Lv K, Luo C . Individual bat virome analysis reveals co-infection and spillover among bats and virus zoonotic potential. Nat Commun. 2023; 14(1):4079. PMC: 10333379. DOI: 10.1038/s41467-023-39835-1. View

20.

Katoh K, Standley D . MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4):772-80. PMC: 3603318. DOI: 10.1093/molbev/mst010. View