The dynamics between limited-term and lifelong coinfecting bacterial parasites in wild rodent hosts

Anat Eidelman, Carmit Cohen, Álvaro Navarro-Castilla, Serina Filler, Ricardo Gutiérrez, Enav Bar-Shira, Naama Shahar, Mario Garrido, Snir Halle, Yoav Romach, Isabel Barja, Séverine Tasker, Shimon Harrus, Aharon Friedman, Hadas Hawlena*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

10 Scopus citations

Abstract

Interactions between coinfecting parasites may take various forms, either direct or indirect, facilitative or competitive, and may be mediated by either bottom-up or top-down mechanisms. Although each form of interaction leads to different evolutionary and ecological outcomes, it is challenging to tease them apart throughout the infection period. To establish the first step towards a mechanistic understanding of the interactions between coinfecting limited-term bacterial parasites and lifelong bacterial parasites, we studied the coinfection of Bartonella sp. (limited-term) and Mycoplasma sp. (lifelong), which commonly co-occur in wild rodents. We infected Bartonella- and Mycoplasma-free rodents with each species, and simultaneously with both, and quantified the infection dynamics and host responses. Bartonella benefited from the interaction; its infection load decreased more slowly in coinfected rodents than in rodents infected with Bartonella alone. There were no indications for bottom-up effects, but coinfected rodents experienced various changes, depending on the infection stage, in their body mass, stress levels and activity pattern, which may further affect bacterial replication and transmission. Interestingly, the infection dynamics and changes in the average coinfected rodent traits were more similar to the chronic effects of Mycoplasma infection, whereas coinfection uniquely impaired the host’s physiological and behavioral stability. These results suggest that parasites with distinct life history strategies may interact, and their interaction may be asymmetric, non-additive, multifaceted and dynamic through time. Because multiple, sometimes contrasting, forms of interactions are simultaneously at play and their relative importance alternates throughout the course of infection, the overall outcome may change under different ecological conditions.

Original languageAmerican English
Article numberjeb203562
JournalJournal of Experimental Biology
Volume222
Issue number15
DOIs
StatePublished - 2019

Bibliographical note

Funding Information:
We thank N. Kronfeld-Schor, M. Einav, Y. Shani, O. Altstein, N. Azran and A. Tsairi for valuable help during this study, and B. Rosental, M. Segoli and Y. Shafran for helpful discussions on early versions of the manuscript. This is publication number 1033 of the Mitrani Department of Desert Ecology. This work was supported by the Israel Science Foundation (1391/15 to H.H. and 688/17 to S.H.). C.C. was sponsored by the short-term postdoctoral fellowship of Ben-Gurion University of the Negev (BGU), and M.G. was sponsored by The Kreitman School of Advanced Graduate Studies (BGU) and the Blaustein Center for Scientific Cooperation (Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev). S.F. holds a PhD studentship at Bristol Veterinary School that is sponsored primarily by the Langford Trust, but also Zoetis Animal Health. The analyses of physiological stress were partially supported by the Etho-Physiology Laboratory (Head of Laboratory, Dr Isabel Barja), Universidad Autónoma de Madrid.

Funding Information:
This work was supported by the Israel Science Foundation (1391/15 to H.H. and 688/17 to S.H.). C.C. was sponsored by the short-term postdoctoral fellowship of Ben-Gurion University of the Negev (BGU), and M.G. was sponsored by The Kreitman School of Advanced Graduate Studies (BGU) and the Blaustein Center for Scientific Cooperation (Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev). S.F. holds a PhD studentship at Bristol Veterinary School that is sponsored primarily by the Langford Trust, but also Zoetis Animal Health. The analyses of physiological stress were partially supported by the Etho-Physiology Laboratory (Head of Laboratory, Dr Isabel Barja), Universidad Autónoma de Madrid.

Publisher Copyright:
© 2019. Published by The Company of Biologists Ltd.

Keywords

  • Coinfection
  • Concomitant infections
  • Mixed infections
  • Multiple parasites
  • Within-host competition
  • Within-host facilitation

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