Combined effects of thermal stress and symbiont identity on carbon flux in a model cnidarian-dinoflagellate symbiosis

IF 1.8 3区 生物学 Q3 ECOLOGY
Evan M. Heit, Simon K. Davy
{"title":"Combined effects of thermal stress and symbiont identity on carbon flux in a model cnidarian-dinoflagellate symbiosis","authors":"Evan M. Heit,&nbsp;Simon K. Davy","doi":"10.1016/j.jembe.2024.152009","DOIUrl":null,"url":null,"abstract":"<div><p>Reef corals rely on their symbiotic relationship with dinoflagellates of the family Symbiodiniaceae for their metabolic energy demands, but this relationship is sensitive to thermal stress which can induce bleaching. We investigated the flux of <sup>14</sup>C-labeled photosynthate in the sea anemone <em>Exaiptasia diaphana</em> (‘Aiptasia’) - a model for the cnidarian-dinoflagellate symbiosis - under low, control and high temperatures (15, 25, 33 °C) when colonized by either its native symbiont <em>Breviolum minutum</em> or the non-native but thermally tolerant <em>Durusdinium trenchii</em> or <em>Breviolum psygmophilum. B. psygmophilum</em> formed the most thermally stable symbiosis, maintaining a higher population density, and fixing and translocating similar or more carbon than the other two species at both high and low temperatures. In contrast, anemones containing <em>D. trenchii</em> markedly bleached at both high and low temperatures, confirming the sensitivity of this host-symbiont pairing to thermal extremes. Elevated temperature led to a significant increase in the percentage of fixed carbon (%) translocated from the symbiont to the host with both <em>Breviolum</em> species, however the total amount of carbon released to the host by the symbiont population (translocated C <em>per</em> mg of host protein) remained consistent between elevated and control temperatures due to the reduced rate of total photosynthetic carbon fixation. The highest rates of photosynthesis and carbon translocation by the symbiont population were seen at the low temperature, reflecting the maintenance or elevation of photosynthesis and/or symbiont density relative to the control. Overall, our findings underscore the significance of symbiont identity in conjunction with host-symbiont specificity in dictating the thermal resilience of the cnidarian-dinoflagellate symbiosis and emphasizing the potential of <em>B. psygmophilum</em> as an interesting candidate for future studies.</p></div>","PeriodicalId":50197,"journal":{"name":"Journal of Experimental Marine Biology and Ecology","volume":"575 ","pages":"Article 152009"},"PeriodicalIF":1.8000,"publicationDate":"2024-04-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Experimental Marine Biology and Ecology","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0022098124000248","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"ECOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Reef corals rely on their symbiotic relationship with dinoflagellates of the family Symbiodiniaceae for their metabolic energy demands, but this relationship is sensitive to thermal stress which can induce bleaching. We investigated the flux of 14C-labeled photosynthate in the sea anemone Exaiptasia diaphana (‘Aiptasia’) - a model for the cnidarian-dinoflagellate symbiosis - under low, control and high temperatures (15, 25, 33 °C) when colonized by either its native symbiont Breviolum minutum or the non-native but thermally tolerant Durusdinium trenchii or Breviolum psygmophilum. B. psygmophilum formed the most thermally stable symbiosis, maintaining a higher population density, and fixing and translocating similar or more carbon than the other two species at both high and low temperatures. In contrast, anemones containing D. trenchii markedly bleached at both high and low temperatures, confirming the sensitivity of this host-symbiont pairing to thermal extremes. Elevated temperature led to a significant increase in the percentage of fixed carbon (%) translocated from the symbiont to the host with both Breviolum species, however the total amount of carbon released to the host by the symbiont population (translocated C per mg of host protein) remained consistent between elevated and control temperatures due to the reduced rate of total photosynthetic carbon fixation. The highest rates of photosynthesis and carbon translocation by the symbiont population were seen at the low temperature, reflecting the maintenance or elevation of photosynthesis and/or symbiont density relative to the control. Overall, our findings underscore the significance of symbiont identity in conjunction with host-symbiont specificity in dictating the thermal resilience of the cnidarian-dinoflagellate symbiosis and emphasizing the potential of B. psygmophilum as an interesting candidate for future studies.

热应力和共生体特性对模型刺胞动物-鞭毛虫共生中碳通量的综合影响
珊瑚礁依靠与共生藻科甲藻的共生关系来满足新陈代谢的能量需求,但这种关系对热应力很敏感,而热应力会诱发白化现象。我们研究了海葵 Exaiptasia diaphana("Aiptasia")--刺丝胞动物与双鞭毛藻共生的模型--在低温、控制温度和高温(15、25、33 °C)条件下,当被其原生共生体 Breviolum minutum 或非原生但耐高温的 Durusdinium trenchii 或 Breviolum psygmophilum 定殖时,14C 标记的光合成代谢物的通量。B. psygmophilum 形成了最稳定的热共生关系,能维持较高的种群密度,在高温和低温条件下的碳固定和转移量与其他两个物种相似或更多。相比之下,含有海沟藻的海葵在高温和低温条件下都明显白化,这证实了这种宿主-共生体配对对极端温度的敏感性。温度升高导致共生体向宿主转运的固定碳百分比(%)显著增加,但由于光合作用碳固定的总速率降低,共生体向宿主释放的碳总量(每毫克宿主蛋白质转运的碳)在升高温度和控制温度下保持一致。在低温条件下,共生体群体的光合作用和碳转运速率最高,这反映出光合作用和/或共生体密度相对于对照组保持或有所提高。总之,我们的研究结果强调了共生体特性与宿主-共生体特异性在决定刺胞动物-鞭毛虫共生的热适应性方面的重要作用,并强调了嗜潮虫作为未来研究对象的潜力。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Journal of Experimental Marine Biology and Ecology
Journal of Experimental Marine Biology and Ecology 生物-海洋与淡水生物学
CiteScore
4.30
自引率
0.00%
发文量
98
审稿时长
14 weeks
期刊介绍: The Journal of Experimental Marine Biology and Ecology provides a forum for experimental ecological research on marine organisms in relation to their environment. Topic areas include studies that focus on biochemistry, physiology, behavior, genetics, and ecological theory. The main emphasis of the Journal lies in hypothesis driven experimental work, both from the laboratory and the field. Natural experiments or descriptive studies that elucidate fundamental ecological processes are welcome. Submissions should have a broad ecological framework beyond the specific study organism or geographic region. Short communications that highlight emerging issues and exciting discoveries within five printed pages will receive a rapid turnaround. Papers describing important new analytical, computational, experimental and theoretical techniques and methods are encouraged and will be highlighted as Methodological Advances. We welcome proposals for Review Papers synthesizing a specific field within marine ecology. Finally, the journal aims to publish Special Issues at regular intervals synthesizing a particular field of marine science. All printed papers undergo a peer review process before being accepted and will receive a first decision within three months.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信