Abstract:Metacaspases are a subgroup of caspase homologues represented in bacteria, algae and plants. Although type I and type II metacaspases are present in plants, recently discovered and uncharacterized type III metacaspases can only be found in algae which have undergone secondary endosymbiosis. We analysed the expression levels of all 13 caspase homologues in the cryptophyte Guillardia theta in vivo and biochemically characterized its only type III metacaspase, GtMC2, in vitro. Type III metacaspase GtMC2 was shown… Show more
“…A large number of metacaspases‐like genes are common in diazotrophic filamentous cyanobacteria. Nine metacaspases are found in Anabaena variabilis ATCC 29413, nine in Nostoc punctiforme while in the T. erythraeum IMS101 genome 12 TeMC have been identified (Jiang et al ., ; Asplund‐Samuelsson, ; Klemenčič and Funk, ); cumulatively representing 0.22% of total encoded proteome (Jiang et al ., ). We analysed the domain structures of the 12 TeMC proteins provide to additional context to their secondary structure and obtain possible clues for their cellular function.…”
Section: Resultsmentioning
confidence: 99%
“…The highest number of metacaspases from all cyanobacteria analysed to date are found in the marine diazotrophic Trichodesmium genome which contains 12 metacaspases (Jiang et al ., ; Asplund‐Samuelsson et al ., ; ). Due to the lack of the P10 domain in their sequence, metacaspases in prokaryotes are termed metacaspase‐like proteins or at other times orthocaspases (Choi and Berges, ; Klemenčič et al ., ; Klemenčič and Funk, ). Here, we use the term TeMC to describe Trichodesmium metacaspase‐like (TeMC) proteases.…”
Summary
Metacaspases are cysteine specific proteases implicated in cell‐signalling, stress acclimation and programmed cell death (PCD) pathways in plants, fungi, protozoa, bacteria and algae. We investigated metacaspase‐like gene expression and biochemical activity in the bloom‐forming, N2‐fixing, marine cyanobacterium Trichodesmium, which undergoes PCD under low iron and high‐light stress. We examined these patterns with respect to in‐silico analyses of protein domain architectures that revealed a diverse array of regulatory domains within Trichodesmium metacaspases‐like (TeMC) proteins. Experimental manipulations of laboratory cultures and oceanic surface blooms of Trichodesmium from the South Pacific Ocean triggered PCD under Fe‐limitation and high light along with enhanced TeMC activity and upregulated expression of diverse TeMC representatives containing different regulatory domains. Furthermore, TeMC activity was significantly and positively correlated with caspase‐like activity, which has been routinely observed to increase with PCD induction in Trichodesmium. Although both TeMC and caspase‐like activities were stimulated upon PCD induction, inhibitor treatments of these proteolytic activities provided further evidence of largely distinct substrate specificities, even though some inhibitory crossover was observed. Our findings are the first results linking metacaspase expression and activity in PCD induced mortality in Trichodesmium. Yet, the role/s and specific activities of these different proteins remain to be elucidated.
“…A large number of metacaspases‐like genes are common in diazotrophic filamentous cyanobacteria. Nine metacaspases are found in Anabaena variabilis ATCC 29413, nine in Nostoc punctiforme while in the T. erythraeum IMS101 genome 12 TeMC have been identified (Jiang et al ., ; Asplund‐Samuelsson, ; Klemenčič and Funk, ); cumulatively representing 0.22% of total encoded proteome (Jiang et al ., ). We analysed the domain structures of the 12 TeMC proteins provide to additional context to their secondary structure and obtain possible clues for their cellular function.…”
Section: Resultsmentioning
confidence: 99%
“…The highest number of metacaspases from all cyanobacteria analysed to date are found in the marine diazotrophic Trichodesmium genome which contains 12 metacaspases (Jiang et al ., ; Asplund‐Samuelsson et al ., ; ). Due to the lack of the P10 domain in their sequence, metacaspases in prokaryotes are termed metacaspase‐like proteins or at other times orthocaspases (Choi and Berges, ; Klemenčič et al ., ; Klemenčič and Funk, ). Here, we use the term TeMC to describe Trichodesmium metacaspase‐like (TeMC) proteases.…”
Summary
Metacaspases are cysteine specific proteases implicated in cell‐signalling, stress acclimation and programmed cell death (PCD) pathways in plants, fungi, protozoa, bacteria and algae. We investigated metacaspase‐like gene expression and biochemical activity in the bloom‐forming, N2‐fixing, marine cyanobacterium Trichodesmium, which undergoes PCD under low iron and high‐light stress. We examined these patterns with respect to in‐silico analyses of protein domain architectures that revealed a diverse array of regulatory domains within Trichodesmium metacaspases‐like (TeMC) proteins. Experimental manipulations of laboratory cultures and oceanic surface blooms of Trichodesmium from the South Pacific Ocean triggered PCD under Fe‐limitation and high light along with enhanced TeMC activity and upregulated expression of diverse TeMC representatives containing different regulatory domains. Furthermore, TeMC activity was significantly and positively correlated with caspase‐like activity, which has been routinely observed to increase with PCD induction in Trichodesmium. Although both TeMC and caspase‐like activities were stimulated upon PCD induction, inhibitor treatments of these proteolytic activities provided further evidence of largely distinct substrate specificities, even though some inhibitory crossover was observed. Our findings are the first results linking metacaspase expression and activity in PCD induced mortality in Trichodesmium. Yet, the role/s and specific activities of these different proteins remain to be elucidated.
“…As expected, caspases are regulated through the post‐translational regulation of their activity as many of these genes are constitutively expressed (Fuentes‐Prior and Salvesen, ). When whole‐genome sequences became available over the past two decades, it was apparent that caspases have evolved specifically in the animal kingdom, and structurally related proteases called metacaspases (MCs) exist in other phyla that extend back to single‐cell eukaryotes, such as microalgae and fungi (Tsiatsiani et al ., ; Klemencic and Funk, ). Related genes encoding metacaspase‐like proteases with a conserved p20 domain that has catalytic motifs related to MCs have also been identified in sequenced genomes of many eubacteria and archaea, thus implicating their evolution from prokaryotic ancestors (Asplund‐Samuelsson et al ., ).…”
Section: Introductionmentioning
confidence: 99%
“…Although the results from loss‐of‐function analysis with several MC‐encoding genes in yeast and plants are consistent with their role in regulating PCD and stress responses, analogous to the case of caspases in animals, there are also interesting distinctions found between them. One key difference is that all three types of MCs that have been identified and characterized prefer target sites with a basic amino acid residue (arginine or lysine) at the P1 position instead of an aspartate, as in the case for caspases (Vercammen et al ., ; Zhang and Lam, ; Klemencic and Funk, ). Structural studies of type‐I MCs from yeast and protozoa also demonstrated that these enzymes function as monomers instead of dimers in the case of caspases (McLuskey et al ., ; Wong et al ., ).…”
Type-II metacaspases are conserved cysteine proteases found in eukaryotes with oxygenic photosynthesis, including green plants and some algae, such as Chlamydomonas and Volvox. Genetic and biochemical studies showed that some members in this protease family could be involved in oxidative stress-induced cell death in higher plants, but their regulatory mechanisms remain unclear. Biochemically, two distinct classes of type-II metacaspases are exemplified by AtMC4 and AtMC9 from Arabidopsis, with AtMC4 activation dependent on calcium under neutral pH, whereas AtMC9 is active only under mildly acidic pH, regardless of the availability of calcium. Here, we constructed all six possible combinations between the p20, linker, and p10 domains from AtMC4 and AtMC9. Our results show that calcium stimulation of AtMC4 activity is associated with essential amino acids located in its p20 domain. In contrast, the acidic pH optimum trait is lost from AtMC9 if one or two of its domains are replaced by that from AtMC4, suggesting that multiple interactions between domains in AtMC9 may be responsible for this property. Consistent with this, we found conserved 'signature' residues in each of the three domains that distinguish AtMC4- and AtMC9-like classes of metacaspases. Tracing the origin of the AtMC9 class, we found evidence for its appearance between lycophytes and gymnosperms, coincident with the evolution of more complex root archetypes in terrestrial plants. Our work suggests that the distinctive properties of the AtMC9-like protease could be associated with special cellular physiology in the roots of gymnosperms and angiosperms that are distinct from lycophytes.
“…As the regulatory modes of type I and II metacaspases are uncovered, the development of sequencing technologies gives access to genes encoding other types of metacaspases in other organisms. For example, through a bioinformatic analysis, Klemenčič & Funk (in this issue, pp. 1179–1191) discuss a type III metacaspase, named GtMC2, in the cryptophyte Guillardia theta .…”
This article is a Commentary on Schaller et al. (pp. 901–915), Liu & Moschou (pp. 916–922), James et al. (pp. 923–928), Dissmeyer et al. (pp. 929–935), Demir et al. (pp. 936–943), Zhang et al. (pp. 1106–1126), Radchuk et al. (pp. 1127–1142), Cai et al. (pp. 1143–1155), Lema Asqui et al. (pp. 1156–1166), Beloshistov et al. (pp. 1167–1178) and Klemenčič & Funk (pp. 1179–1191), all of which are published in this issue.
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