Abstract:Reactive oxygen species (ROS) such as superoxide and hydrogen peroxide are by-products of various metabolic processes in aerobic organisms including Euglena. Chloroplasts and mitochondria are the main sites of ROS generation by photosynthesis and respiration, respectively, through the active electron transport chain. An efficient antioxidant network is required to maintain intracellular ROS pools at optimal conditions for redox homeostasis. A comparison with the networks of plants and animals revealed that Eug… Show more
“…Intriguingly, despite their apparent importance, catalases are not essential for life [59] and there are examples of eukaryote organisms lacking these enzymes (e.g. Euglena spp., Neurospora crassa ) [61]. It has, furthermore, been documented that catalase null mice develop normally and do not display any gross physical or behavioral abnormalities [62].…”
Background
Tardigrades are renowned for their ability to enter cryptobiosis (latent life) and endure extreme stress, including desiccation and freezing. Increased focus is on revealing molecular mechanisms underlying this tolerance. Here, we provide the first transcriptomes from the heterotardigrade
Echiniscoides
cf.
sigismundi
and the eutardigrade
Richtersius
cf.
coronifer
, and compare these with data from other tardigrades and six eukaryote models. Investigating 107 genes/gene families, our study provides a thorough analysis of tardigrade gene content with focus on stress tolerance.
Results
E.
cf.
sigismundi
, a strong cryptobiont, apparently lacks expression of a number of stress related genes. Most conspicuous is the lack of transcripts from genes involved in classical Non-Homologous End Joining. Our analyses suggest that post-cryptobiotic survival in tardigrades could rely on high fidelity transcription-coupled DNA repair. Tardigrades seem to lack many peroxins, but they all have a comprehensive number of genes encoding proteins involved in antioxidant defense. The “tardigrade unique proteins” (CAHS, SAHS, MAHS, RvLEAM), seem to be missing in the heterotardigrade lineage, revealing that cryptobiosis in general cannot be attributed solely to these proteins. Our investigation further reveals a unique and highly expressed cold shock domain. We hypothesize that the cold shock protein acts as a RNA-chaperone involved in regulation of translation following freezing.
Conclusions
Our results show common gene family contractions and expansions within stress related gene pathways in tardigrades, but also indicate that evolutionary lineages have a high degree of divergence. Different taxa and lineages may exhibit unique physiological adaptations towards stress conditions involving possible unknown functional homologues and/or novel physiological and biochemical mechanisms. To further substantiate the current results genome assemblies coupled with transcriptome data and experimental investigations are needed from tardigrades belonging to different evolutionary lineages.
Electronic supplementary material
The online version of this article (10.1186/s12864-019-5912-x) contains supplementary material, which is available to authorized users.
“…Intriguingly, despite their apparent importance, catalases are not essential for life [59] and there are examples of eukaryote organisms lacking these enzymes (e.g. Euglena spp., Neurospora crassa ) [61]. It has, furthermore, been documented that catalase null mice develop normally and do not display any gross physical or behavioral abnormalities [62].…”
Background
Tardigrades are renowned for their ability to enter cryptobiosis (latent life) and endure extreme stress, including desiccation and freezing. Increased focus is on revealing molecular mechanisms underlying this tolerance. Here, we provide the first transcriptomes from the heterotardigrade
Echiniscoides
cf.
sigismundi
and the eutardigrade
Richtersius
cf.
coronifer
, and compare these with data from other tardigrades and six eukaryote models. Investigating 107 genes/gene families, our study provides a thorough analysis of tardigrade gene content with focus on stress tolerance.
Results
E.
cf.
sigismundi
, a strong cryptobiont, apparently lacks expression of a number of stress related genes. Most conspicuous is the lack of transcripts from genes involved in classical Non-Homologous End Joining. Our analyses suggest that post-cryptobiotic survival in tardigrades could rely on high fidelity transcription-coupled DNA repair. Tardigrades seem to lack many peroxins, but they all have a comprehensive number of genes encoding proteins involved in antioxidant defense. The “tardigrade unique proteins” (CAHS, SAHS, MAHS, RvLEAM), seem to be missing in the heterotardigrade lineage, revealing that cryptobiosis in general cannot be attributed solely to these proteins. Our investigation further reveals a unique and highly expressed cold shock domain. We hypothesize that the cold shock protein acts as a RNA-chaperone involved in regulation of translation following freezing.
Conclusions
Our results show common gene family contractions and expansions within stress related gene pathways in tardigrades, but also indicate that evolutionary lineages have a high degree of divergence. Different taxa and lineages may exhibit unique physiological adaptations towards stress conditions involving possible unknown functional homologues and/or novel physiological and biochemical mechanisms. To further substantiate the current results genome assemblies coupled with transcriptome data and experimental investigations are needed from tardigrades belonging to different evolutionary lineages.
Electronic supplementary material
The online version of this article (10.1186/s12864-019-5912-x) contains supplementary material, which is available to authorized users.
“…Unlike non-selenium GPXs from Chlorophyta, non-selenium GPX isolated from E. gracilis uses GSH as an electron donor [111]. In addition to GSH-dependent GPX, the transcriptome data of E. gracilis indicated the existence of three putative Trxdependent GPXs [112].…”
“…Its biosynthesis is catalyzed by two distinct enzymes: glutathionylspermidine (GSP) synthetase (GSPS) conjugates the first GSH molecule to spermidine, and trypanothione synthetase (TRYS) adds the second GSH molecule to GSP (Figure 4) [128]. Transcriptome data showed that E. gracilis contains two highly homologous genes to GSPS and TRYS genes from trypanosomatid Crithidia fasciculata [112]; however, these genes have not yet been functionally characterized.…”
“…In E. gracilis, the TRYR enzyme was purified from algal cells and biochemically characterized [132]. Genes encoding putative TRYR and TXN were identified in the E. gracilis transcriptome data [112]. Moreover, knockdown of TRYR genes in E. gracilis inhibited growth, suggesting a functional T(SH) 2 system in this algal species [133].…”
Eukaryotic microalgae have been classified into several biological divisions and have evolutionarily acquired diverse morphologies, metabolisms, and life cycles. They are naturally exposed to environmental stresses that cause oxidative damage due to reactive oxygen species accumulation. To cope with environmental stresses, microalgae contain various antioxidants, including carotenoids, ascorbate (AsA), and glutathione (GSH). Carotenoids are hydrophobic pigments required for light harvesting, photoprotection, and phototaxis. AsA constitutes the AsA-GSH cycle together with GSH and is responsible for photooxidative stress defense. GSH contributes not only to ROS scavenging, but also to heavy metal detoxification and thiol-based redox regulation. The evolutionary diversity of microalgae influences the composition and biosynthetic pathways of these antioxidants. For example, α-carotene and its derivatives are specific to Chlorophyta, whereas diadinoxanthin and fucoxanthin are found in Heterokontophyta, Haptophyta, and Dinophyta. It has been suggested that AsA is biosynthesized via the plant pathway in Chlorophyta and Rhodophyta and via the Euglena pathway in Euglenophyta, Heterokontophyta, and Haptophyta. The GSH biosynthetic pathway is conserved in all biological kingdoms; however, Euglenophyta are able to synthesize an additional thiol antioxidant, trypanothione, using GSH as the substrate. In the present study, we reviewed and discussed the diversity of microalgal antioxidants, including recent findings.
“…These genes are also absent or nonfunctional in trypanosomatid parasitic protists, such as Leishmania [25]. In addition, Trypanosomatids produce the unusual GSH molecule trypanothione and express trypanothione-dependent reductase and peroxidase enzymes that function analogously to GR and GPX in trypanothione redox cycling [26,27]. Insects largely lack the GR and GPX genes and so, although they rely on the GSH redox cycle, GSH is regenerated via the TRX system rather than GR.…”
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.
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