Diverse fates of ancient horizontal gene transfers in extremophilic red algae

IF 4.3 2区 生物学 Q2 MICROBIOLOGY Environmental microbiology Pub Date : 2024-05-02 DOI:10.1111/1462-2920.16629
Julia Van Etten, Timothy G. Stephens, Erin Chille, Anna Lipzen, Daniel Peterson, Kerrie Barry, Igor V. Grigoriev, Debashish Bhattacharya
{"title":"Diverse fates of ancient horizontal gene transfers in extremophilic red algae","authors":"Julia Van Etten,&nbsp;Timothy G. Stephens,&nbsp;Erin Chille,&nbsp;Anna Lipzen,&nbsp;Daniel Peterson,&nbsp;Kerrie Barry,&nbsp;Igor V. Grigoriev,&nbsp;Debashish Bhattacharya","doi":"10.1111/1462-2920.16629","DOIUrl":null,"url":null,"abstract":"<p>Horizontal genetic transfer (HGT) is a common phenomenon in eukaryotic genomes. However, the mechanisms by which HGT-derived genes persist and integrate into other pathways remain unclear. This topic is of significant interest because, over time, the stressors that initially favoured the fixation of HGT may diminish or disappear. Despite this, the foreign genes may continue to exist if they become part of a broader stress response or other pathways. The conventional model suggests that the acquisition of HGT equates to adaptation. However, this model may evolve into more complex interactions between gene products, a concept we refer to as the ‘Integrated HGT Model’ (IHM). To explore this concept further, we studied specialized HGT-derived genes that encode heavy metal detoxification functions. The recruitment of these genes into other pathways could provide clear examples of IHM. In our study, we exposed two anciently diverged species of polyextremophilic red algae from the <i>Galdieria</i> genus to arsenic and mercury stress in laboratory cultures. We then analysed the transcriptome data using differential and coexpression analysis. Our findings revealed that mercury detoxification follows a ‘one gene-one function’ model, resulting in an indivisible response. In contrast, the <i>ars</i>H gene in the arsenite response pathway demonstrated a complex pattern of duplication, divergence and potential neofunctionalization, consistent with the IHM. Our research sheds light on the fate and integration of ancient HGTs, providing a novel perspective on the ecology of extremophiles.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":null,"pages":null},"PeriodicalIF":4.3000,"publicationDate":"2024-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16629","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Environmental microbiology","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/1462-2920.16629","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Horizontal genetic transfer (HGT) is a common phenomenon in eukaryotic genomes. However, the mechanisms by which HGT-derived genes persist and integrate into other pathways remain unclear. This topic is of significant interest because, over time, the stressors that initially favoured the fixation of HGT may diminish or disappear. Despite this, the foreign genes may continue to exist if they become part of a broader stress response or other pathways. The conventional model suggests that the acquisition of HGT equates to adaptation. However, this model may evolve into more complex interactions between gene products, a concept we refer to as the ‘Integrated HGT Model’ (IHM). To explore this concept further, we studied specialized HGT-derived genes that encode heavy metal detoxification functions. The recruitment of these genes into other pathways could provide clear examples of IHM. In our study, we exposed two anciently diverged species of polyextremophilic red algae from the Galdieria genus to arsenic and mercury stress in laboratory cultures. We then analysed the transcriptome data using differential and coexpression analysis. Our findings revealed that mercury detoxification follows a ‘one gene-one function’ model, resulting in an indivisible response. In contrast, the arsH gene in the arsenite response pathway demonstrated a complex pattern of duplication, divergence and potential neofunctionalization, consistent with the IHM. Our research sheds light on the fate and integration of ancient HGTs, providing a novel perspective on the ecology of extremophiles.

Abstract Image

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
嗜极红藻中古老水平基因转移的不同命运
水平基因转移(HGT)是真核生物基因组中的一种常见现象。然而,HGT 衍生基因持续存在并整合到其他途径的机制仍不清楚。这个话题之所以引起人们的极大兴趣,是因为随着时间的推移,最初有利于 HGT 固定的压力因素可能会减少或消失。尽管如此,如果外来基因成为更广泛的应激反应或其他途径的一部分,它们可能会继续存在。传统模式认为,获得 HGT 就等于适应。然而,这种模式可能会演变为基因产物之间更复杂的相互作用,我们将这种概念称为 "综合 HGT 模式"(IHM)。为了进一步探索这一概念,我们研究了编码重金属解毒功能的特化 HGT 衍生基因。这些基因被招募到其他通路中,可以提供清晰的 IHM 例子。在我们的研究中,我们在实验室培养物中让两种古老分化的嗜极性红藻(Galdieria)受到砷和汞的胁迫。然后,我们利用差异和共表达分析方法对转录组数据进行了分析。我们的研究结果表明,汞解毒遵循 "一基因一功能 "模式,从而产生不可分割的反应。相比之下,亚砷酸盐反应途径中的 arsH 基因则表现出复制、分化和潜在新功能化的复杂模式,与 IHM 模式一致。我们的研究揭示了古老 HGTs 的命运和整合,为研究嗜极生物的生态学提供了一个新的视角。
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 去求助
来源期刊
Environmental microbiology
Environmental microbiology 环境科学-微生物学
CiteScore
9.90
自引率
3.90%
发文量
427
审稿时长
2.3 months
期刊介绍: Environmental Microbiology provides a high profile vehicle for publication of the most innovative, original and rigorous research in the field. The scope of the Journal encompasses the diversity of current research on microbial processes in the environment, microbial communities, interactions and evolution and includes, but is not limited to, the following: the structure, activities and communal behaviour of microbial communities microbial community genetics and evolutionary processes microbial symbioses, microbial interactions and interactions with plants, animals and abiotic factors microbes in the tree of life, microbial diversification and evolution population biology and clonal structure microbial metabolic and structural diversity microbial physiology, growth and survival microbes and surfaces, adhesion and biofouling responses to environmental signals and stress factors modelling and theory development pollution microbiology extremophiles and life in extreme and unusual little-explored habitats element cycles and biogeochemical processes, primary and secondary production microbes in a changing world, microbially-influenced global changes evolution and diversity of archaeal and bacterial viruses new technological developments in microbial ecology and evolution, in particular for the study of activities of microbial communities, non-culturable microorganisms and emerging pathogens
期刊最新文献
Understanding the ecological versatility of Tetracladium species in temperate forest soils Issue Information Production and utilization of pseudocobalamin in marine Synechococcus cultures and communities Cable bacteria colonise new sediment environments through water column dispersal Novel oil-associated bacteria in Arctic seawater exposed to different nutrient biostimulation regimes
×
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
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 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 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1