Divergent functions of two clades of flavodoxin in diatoms mitigate oxidative stress and iron limitation
- University of Washington, United States
Abstract
Phytoplankton rely on diverse mechanisms to adapt to the decreased iron bioavailability and oxidative stress-inducing conditions of today's oxygenated oceans, including replacement of the iron-requiring ferredoxin electron shuttle protein with a less-efficient iron-free flavodoxin under iron limiting conditions. And yet, diatoms transcribe flavodoxins in high-iron regions in contrast to other phytoplankton. Here, we show that the two clades of flavodoxins present within diatoms exhibit a functional divergence, with only clade II flavodoxins displaying the canonical role in acclimation to iron limitation. We created CRISPR/Cas9 knock-outs of the clade I flavodoxin from the model diatom Thalassiosira pseudonana and found these cell lines are hypersensitive to oxidative stress, while maintaining a wild-type response to iron limitation. Within natural diatom communities, clade I flavodoxin transcript abundance is regulated over the diel cycle rather than in response to iron availability, whereas clade II transcript abundances increase either in iron‑limiting regions or under artificially induced iron-limitation. The observed functional specialization of two flavodoxin variants within diatoms reiterates two major stressors associated with contemporary oceans and illustrates diatom strategies to flourish in diverse aquatic ecosystems.
Data availability
Sequencing data from cultures have been deposited in GEO under accession code GSE217467. All other relevant data supporting the findings of the study are available in this article and its Supplementary files.
-
Five diatoms transcriptomes under iron limitation and oxidative stressNCBI Gene Expression Omnibus, GSE217467.
-
Diel Eukaryotic Metatranscriptomes from the North Pacific Subtropical GyreNCBI Sequence Read Archive under BioProject ID PRJNA492142.
-
Eukaryotic Metatranscriptomes from the North Pacific Ocean (Gradients 1)NCBI Sequence Read Archive under BioProject PRJNA690573.
-
On-deck Incubation Eukaryotic Metatranscriptomes (Gradients 2)NCBI Sequence Read Archive under BioProject PRJNA690575.
Article and author information
Author details
Shiri Graff van Creveld
E Virginia Armbrust
Funding
Simons Foundation (426570SP)
- E Virginia Armbrust
Simons Foundation (721244)
- E Virginia Armbrust
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2023, Graff van Creveld et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 667
- views
-
- 87
- downloads
-
- 6
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Divergent functions of two clades of flavodoxin in diatoms mitigate oxidative stress and iron limitation
eLife 12:e84392.
https://doi.org/10.7554/eLife.84392
Further reading
-
- Ecology
- Evolutionary Biology
Understanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biased towards colorful species, without similar attention paid to inconspicuous ones that are often assumed to be undefended. As a result, our understanding of how chemical defense evolved in this group is incomplete. Here, we provide new data showing that, in contrast to previous studies, species from each undefended poison frog clade have measurable yet low amounts of alkaloids. We confirm that undefended dendrobatids regularly consume mites and ants, which are known sources of alkaloids. Thus, our data suggest that diet is insufficient to explain the defended phenotype. Our data support the existence of a phenotypic intermediate between toxin consumption and sequestration — passive accumulation — that differs from sequestration in that it involves no derived forms of transport and storage mechanisms yet results in low levels of toxin accumulation. We discuss the concept of passive accumulation and its potential role in the origin of chemical defenses in poison frogs and other toxin-sequestering organisms. In light of ideas from pharmacokinetics, we incorporate new and old data from poison frogs into an evolutionary model that could help explain the origins of acquired chemical defenses in animals and provide insight into the molecular processes that govern the fate of ingested toxins.
-
- Ecology
Tracking wild pigs with GPS devices reveals how their social interactions could influence the spread of disease, offering new strategies for protecting agriculture, wildlife, and human health.
