Comparative Analysis of ROS Network Genes in Extremophile Eukaryotes.

Rafe Lyall,Zoran Nikoloski,Tsanko Gechev

doi:10.3390/ijms21239131

Abstract

The reactive oxygen species (ROS) gene network, consisting of both ROS-generating and detoxifying enzymes, adjusts ROS levels in response to various stimuli. We performed a cross-kingdom comparison of ROS gene networks to investigate how they have evolved across all Eukaryotes, including protists, fungi, plants and animals. We included the genomes of 16 extremotolerant Eukaryotes to gain insight into ROS gene evolution in organisms that experience extreme stress conditions. Our analysis focused on ROS genes found in all Eukaryotes (such as catalases, superoxide dismutases, glutathione reductases, peroxidases and glutathione peroxidase/peroxiredoxins) as well as those specific to certain groups, such as ascorbate peroxidases, dehydroascorbate/monodehydroascorbate reductases in plants and other photosynthetic organisms. ROS-producing NADPH oxidases (NOX) were found in most multicellular organisms, although several NOX-like genes were identified in unicellular or filamentous species. However, despite the extreme conditions experienced by extremophile species, we found no evidence for expansion of ROS-related gene families in these species compared to other Eukaryotes. Tardigrades and rotifers do show ROS gene expansions that could be related to their extreme lifestyles, although a high rate of lineage-specific horizontal gene transfer events, coupled with recent tetraploidy in rotifers, could explain this observation. This suggests that the basal Eukaryotic ROS scavenging systems are sufficient to maintain ROS homeostasis even under the most extreme conditions.

Highlights

The proliferation of early photosynthetic organisms nearly 2.5 billion years ago led to a massive increase in atmospheric oxygen on early Earth [1]
Our analysis focused on reactive oxygen species (ROS) genes found in all Eukaryotes as well as those specific to certain groups, such as ascorbate peroxidases, dehydroascorbate/monodehydroascorbate reductases in plants and other photosynthetic organisms
Genome sequencing projects have been performed on a range of model Eukaryotic species and, over the past few years, genomes from extremotolerant species, resurrection plants, have become available [41,44,45,46,47,48]

Summary

Introduction

The proliferation of early photosynthetic organisms nearly 2.5 billion years ago led to a massive increase in atmospheric oxygen on early Earth [1]. The sensing and maintenance of noncytotoxic ROS levels in early organisms required a complex network of ROS-related genes, ROS scavengers In complex organisms these systems evolved to sense perturbations in basal ROS levels—depending on the origin or species of ROS molecules produced—enabling the use of ROS as signaling molecules [5,6]. Organisms that encounter extreme abiotic stress conditions—such as extremophiles—may need to tolerate far more drastic perturbations to ROS homoeostasis than species in more moderate environments. It is unclear whether the effects of this lifestyle would necessitate changes to the core ROS-related gene networks. The goal of this study was to analyze ROS-related genes in the genomes of diverse Eukaryotes to see if the extremophile lifestyle was associated with changes to any of the core ROS-related gene families

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Discussion

Conclusion