Diverse fates of ancient horizontal gene transfers in extremophilic red algae

Journal Article · 01 May 2024 · Environmental Microbiology

DOI: https://doi.org/10.1111/1462-2920.16629 · OSTI ID:2345258

Van Etten, Julia ^[1]; Stephens, Timothy G. ^[2]; Chille, Erin ^[1]; Lipzen, Anna ^[3]; Peterson, Daniel ^[3]; Barry, Kerrie ^[3]; Grigoriev, Igor V. ^[4]; Bhattacharya, Debashish  ^[2]

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1. Graduate Program in Ecology and Evolution Rutgers, The State University of New Jersey New Brunswick New Jersey USA
2. Department of Biochemistry and Microbiology Rutgers, The State University of New Jersey New Brunswick New Jersey USA
3. U.S. Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory Berkeley California USA
4. U.S. Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory Berkeley California USA, Department of Plant and Microbial Biology University of California, Berkeley Berkeley California USA

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 ars 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.

• Sponsoring Organization: USDOE
• Grant/Contract Number: AC02-05CH11231
• OSTI ID: 2345258
• Alternate ID(s): OSTI ID: 2367422; OSTI ID: 2447942
• Journal Information: Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 5 Vol. 26; ISSN 1462-2912
• Publisher: Wiley-BlackwellCopyright Statement
• Country of Publication: United Kingdom
• Language: English