Patrick T Stillson, Kaisy Martinez, Johnathan Adamson, Arshya Tehrani, Alison Ravenscraft
{"title":"Temperature influences outcomes of an environmentally acquired symbiosis.","authors":"Patrick T Stillson, Kaisy Martinez, Johnathan Adamson, Arshya Tehrani, Alison Ravenscraft","doi":"10.1093/ismejo/wraf056","DOIUrl":null,"url":null,"abstract":"<p><p>Microbial symbioses are essential for many animals, but their outcomes are often context dependent. For example, rising temperatures can disrupt symbioses by eliminating thermally sensitive symbionts. The temperature tolerance of a symbiont may therefore limit the temperature range of its host, but switching to a more thermally tolerant partner could expand this range. Eastern leaf footed bugs (Leptoglossus phyllopus) depend on symbiotic Caballeronia bacteria which they must acquire from the environment early in development. Could this result in intergenerational partner switching that improves host outcomes under changing conditions? As a first step towards answering this question, we tested the hypothesis that host outcomes in this symbiosis vary among symbiont strains in a temperature-dependent manner. Nymphs were provided with one of six Caballeronia strains with varying thermal optima and reared at temperatures from 24 - 40°C. We observed temperature- and strain-dependent tradeoffs in host outcomes, with different strains conferring improved host weight, development time, and survival at cooler versus warmer temperatures. Differences in host outcomes were most pronounced at high temperatures, with some strains imposing severe costs. However, Caballeronia's in vitro thermal optima did not predict in vivo outcomes. Regardless, strain - and temperature - dependent outcomes suggest that environmental symbiont acquisition could mitigate the effects of thermal stress on host populations. It is often assumed that vertical transmission of a beneficial symbiont from parent to offspring is the optimal strategy, but our results suggest that environmental acquisition could offer unique benefits under changing conditions.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8000,"publicationDate":"2025-03-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"ISME Journal","FirstCategoryId":"93","ListUrlMain":"https://doi.org/10.1093/ismejo/wraf056","RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"ECOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Microbial symbioses are essential for many animals, but their outcomes are often context dependent. For example, rising temperatures can disrupt symbioses by eliminating thermally sensitive symbionts. The temperature tolerance of a symbiont may therefore limit the temperature range of its host, but switching to a more thermally tolerant partner could expand this range. Eastern leaf footed bugs (Leptoglossus phyllopus) depend on symbiotic Caballeronia bacteria which they must acquire from the environment early in development. Could this result in intergenerational partner switching that improves host outcomes under changing conditions? As a first step towards answering this question, we tested the hypothesis that host outcomes in this symbiosis vary among symbiont strains in a temperature-dependent manner. Nymphs were provided with one of six Caballeronia strains with varying thermal optima and reared at temperatures from 24 - 40°C. We observed temperature- and strain-dependent tradeoffs in host outcomes, with different strains conferring improved host weight, development time, and survival at cooler versus warmer temperatures. Differences in host outcomes were most pronounced at high temperatures, with some strains imposing severe costs. However, Caballeronia's in vitro thermal optima did not predict in vivo outcomes. Regardless, strain - and temperature - dependent outcomes suggest that environmental symbiont acquisition could mitigate the effects of thermal stress on host populations. It is often assumed that vertical transmission of a beneficial symbiont from parent to offspring is the optimal strategy, but our results suggest that environmental acquisition could offer unique benefits under changing conditions.
期刊介绍:
The ISME Journal covers the diverse and integrated areas of microbial ecology. We encourage contributions that represent major advances for the study of microbial ecosystems, communities, and interactions of microorganisms in the environment. Articles in The ISME Journal describe pioneering discoveries of wide appeal that enhance our understanding of functional and mechanistic relationships among microorganisms, their communities, and their habitats.