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The Iron-Sulfur Scaffold Protein HCF101 Unveils the Complexity of Organellar Evolution in SAR, Haptista and Cryptista

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The Iron-Sulfur Scaffold Protein HCF101 Unveils the Complexity of Organellar Evolution in SAR, Haptista and Cryptista The Iron-Sulfur Scaffold Protein HCF101 Unveils The Complexity of Organellar Evolution in SAR, Haptista and Cryptista Jan Pyrih Charles University Faculty of Science: Univerzita Karlova Prirodovedecka fakulta Vojtech Žárský Charles University Faculty of Science: Univerzita Karlova Prirodovedecka fakulta Jastin D. Fellow University of Georgia Christopher Grosche University of Marburg: Philipps-Universitat Marburg Dorota Wloga Nencki Institute of Experimental Biology: Instytut Biologii Doswiadczalnej im M Nenckiego Polskiej Akademii Nauk Boris Striepen University of Georgia Uwe G. Maier University of Marburg: Philipps-Universitat Marburg Jan Tachezy ( [email protected] ) Charles University: Univerzita Karlova https://orcid.org/0000-0001-6976-8446 Research article Keywords: HCF101, Ind1, iron-sulfur cluster, mitochondrion, plastid, evolution Posted Date: December 15th, 2020 DOI: https://doi.org/10.21203/rs.3.rs-126638/v1 License: This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full License Version of Record: A version of this preprint was published on March 19th, 2021. See the published version at https://doi.org/10.1186/s12862-021-01777-x. 1 The iron-sulfur scaffold protein HCF101 unveils the complexity of organellar evolution 2 in SAR, Haptista and Cryptista 3 4 Jan Pyriha, Vojtěch Žárskýa, Justin D. Fellowsb, Christopher Groschec,d, Dorota Wlogae, Boris 5 Striepenb, Uwe G. Maierc,d, Jan Tachezya,f. 6 7 a Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Průmyslová 8 595, 252 50 Vestec, Czech Republic. 9 b Department of Cellular Biology, University of Georgia, Athens, Georgia, USA. 10 c Laboratory for Cell Biology, Philipps University Marburg, Karl-von-Frisch-Str. 8, 35032, 11 Marburg, Germany. 12 d LOEWE Center for Synthetic Microbiology (Synmikro), Hans-Meerwein-Str. 6, 35032 13 Marburg, Germany 14 e Laboratory of Cytoskeleton and Cilia Biology, Nencki Institute of Experimental Biology of 15 Polish Academy of Sciences, 3 Pasteur Street, 02-093 Warsaw, Poland. 16 17 18 f To whom correspondence should be addressed: Jan Tachezy, Department of Parasitology, 19 Faculty of Science, Charles University BIOCEV, Průmyslová 595, 252 50 Vestec, Czech 20 Republic. 21 E-mail: [email protected] 1 22 Abstract 23 Background: Nbp35-like proteins (Nbp35, Cfd1, HCF101, Ind1, and AbpC) are P-loop 24 NTPases that serve as components of iron-sulfur cluster (FeS) assembly machineries. In 25 eukaryotes, Ind1 is present in mitochondria, and its function is associated with the assembly 26 of FeS clusters in subunits of respiratory Complex I, Nbp35 and Cfd1 are the components of 27 the cytosolic FeS assembly (CIA) pathway, and HCF101 is involved in FeS assembly of 28 photosystem I in plastids of plants (chHCF101). The AbpC protein operates in Bacteria and 29 Archaea. To date, the cellular distribution of these proteins is considered to be highly 30 conserved with only a few exceptions. 31 Results: We searched for the genes of all members of the Nbp35-like protein family and 32 analyzed their targeting sequences. Nbp35 and Cfd1 were predicted to reside in the cytoplasm 33 with some exceptions of Nbp35 localization to the mitochondria; Ind1was found in the 34 mitochondria, and HCF101 was predicted to reside in plastids (chHCF101) of all 35 photosynthetically active eukaryotes. Surprisingly, we found a second HCF101 paralog in all 36 members of Cryptista, Haptista, and SAR that was predicted to predominantly target 37 mitochondria (mHCF101), whereas Ind1 appeared to be absent in these organisms. We also 38 identified a few exceptions, as apicomplexans possess mHCF101 predicted to localize in the 39 cytosol and Nbp35 in the mitochondria. Our predictions were experimentally confirmed in 40 selected representatives of Apicomplexa (Toxoplasma gondii), Stramenopila (Phaeodactylum 41 tricornutum, Thalassiosira pseudonana), and Ciliophora (Tetrahymena thermophila) by 42 tagging proteins with an transgenic reporter. Phylogenetic analysis suggested that chHCF101 43 and mHCF101 evolved from a common ancestral HCF101 independently of the Nbp35/Cfd1 44 and Ind1 proteins. Interestingly, phylogenetic analysis supports rather a lateral gene transfer 45 of ancestral HCF101 from bacteria than its acquisition being associated with either α- 46 proteobacterial or cyanobacterial endosymbionts. 2 47 Conclusion: Our searches for Nbp35-like proteins across eukaryotic lineages revealed that 48 SAR, Haptista, and Cryptista possess mitochondrial HCF-101. Because plastid localization of 49 HCF101 was only known thus far, the discovery of its mitochondrial paralog explains 50 confusion regarding the presence of HCF101 in organisms that possibly lost secondary 51 plastids (e.g., ciliates, Cryptosporidium) or possess reduced nonphotosynthetic plastids 52 (apicomplexans). 53 54 Keywords 55 HCF101, Ind1, iron-sulfur cluster, mitochondrion, plastid, evolution 56 57 Background 58 Iron-sulfur (FeS) cluster assembly pathways are essential for all three domains of life: 59 Bacteria, Archaea, and Eukarya. In eukaryotes, there are three main pathways, which are 60 localized in distinct cellular compartments: mitochondria, plastids, and the cytosol. The 61 organellar pathways were acquired through endosymbiosis of proteobacteria and 62 cyanobacteria that evolved into mitochondria and plastids, respectively [1, 2]. The 63 mitochondrial FeS cluster assembly (ISC) machinery operates in nearly all forms of 64 mitochondria including anaerobic hydrogenosomes [3] and highly reduced mitosomes [4]. 65 The pathway in plastids is called the sulfur utilization factor (SUF) system, which is present 66 in primary [5] as well as secondary plastids [6–8]. The ISC machinery is functionally linked 67 to the third system, the cytosolic FeS cluster assembly (CIA) machinery. Phylogenetic 68 analysis suggested that the CIA pathway was present in the last eukaryotic common ancestor 69 (LECA) and that its components are predominantly of bacterial origin [9, 10]. There are few 3 70 known exceptions to the highly conserved setup of FeS assembly machineries, and all these 71 exceptions concern protists adapted to anaerobic or microaerobic conditions with modified 72 mitochondria. Archamoebae replaced the ISC pathway with two components of a nitrogen- 73 fixing (NIF) machinery that were acquired by lateral gene transfer (LGT) from ɛ- 74 proteobacteria[11]. The NIF system operates in the cytosol of Entamoeba histolytica or in the 75 cytosol and hydrogenosomes of Mastigamoeba balamuthi [12]. Similarly, the breviate 76 Pygsuia biforma apparently replaced the ISC system with an archeal SUF system [13, 14]. 77 Finally, three SUF components (SufC, SufB, and fused protein SufDSU) of bacterial origin 78 were found in the cytosol of the oxymonad Monocercomonoides sp., which lost its 79 mitochondria [15]. 80 The only proteins that are common to the CIA, ISC, and SUF pathways are P-loop 81 NTPases with the ParA domain: Nbp35/Cfd1, Ind1, and high chlorophyll fluorescence 101 82 (HCF101), respectively (hereafter Nbp35-like proteins). In CIA, Nbp35/Cfd proteins serve in 83 the initial phase of FeS assembly as a [4Fe-4S] scaffold using sulfur and iron that are exported 84 from mitochondria [16]. The FeS cluster is then transferred via Nar1 and the 85 Cia1/Cia2/MMS19 targeting complex to apo-proteins. Ind1 serves as a scaffold in later stages 86 of FeS assembly to deliver [4Fe-4S] clusters specifically to the apo-subunits of mitochondrial 87 respiratory complex I, and thus, the presence of Ind1 closely matches the complex I 88 distribution [17]. Its necessity for complex I maturation underlines the presence of Ind1 in 89 hydrogenosomes, in which complex I is reduced to only two FeS subunits [14, 18]. HCF101 90 was shown to transport [4Fe-4S] clusters to photosystem I subunits and heterodimeric 91 ferredoxin-thioredoxin reductase complexes in plastids of Arabidopsis thaliana [19, 20]. 92 It is believed that the cannonical distribution of FeS cluster assembly machineries and 93 thus that of machinery-specific Nbp35-like proteins is highly conserved in eukaryotes, 94 including protists with primary or complex plastids. The latter organelles evolved in 4 95 eukaryotic hosts from eukaryotic symbionts with green (Euglenozoa and 96 Chlorarachniophyceae) or red (Stramenopila, Alveolata, Haptophytes, and Cryptophytes) 97 plastids [21, 22]. These complex plastids are surrounded by three or more membranes and 98 characterized by the presence of a periplastidal compartment, the extremely reduced cytosol 99 of the endosymbiont and, in the case of cryptophytes and chlorarachniophytes, of a remnant 100 nucleus (nucleomorph). Interestingly, the presence of nucleomorph, which is likely dependent 101 on activities of FeS proteins, correlates with the presence of the endosymbiotic CIA, 102 including Nbp35 that is retained in the periplastidial compartment [7] in addition to CIA in 103 the host cytosol. This curious finding further exemplifies the conserved topology of Nbp35 104 and other CIA components. 105 The localization of HCF101 has not been experimentally studied in most eukaryotic 106 lineages. Moreover, because HCF101 is essential for photosystem I and consequently 107 photosynthesis, it could be particularly interesting to investigate its presence and cellular 108 localization in organisms that possess non-photosynthesizing plastids such as the apicoplast in 109 apicomplexans. The genes for HCF101 have been noticed in several apicomplexan genomes 110 such as Toxoplasma
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