In most eukaryotic phototrophs, the entire heme synthesis is localized to the plastid, and enzymes of cyanobacterial origin dominate the pathway. Despite that, porphobilinogen deaminase (PBGD), the enzyme responsible for the synthesis of hydroxymethybilane in the plastid, shows phylogenetic affiliation to α-proteobacteria, the supposed ancestor of mitochondria. Surprisingly, no PBGD of such origin is found in the heme pathway of the supposed partners of the primary plastid endosymbiosis, a primarily heterotrophic eukaryote, and a cyanobacterium. It appears that α-proteobacterial PBGD is absent from glaucophytes but is present in rhodophytes, chlorophytes, plants, and most algae with complex plastids. This may suggest that in eukaryotic phototrophs, except for glaucophytes, either the gene from the mitochondrial ancestor was retained while the cyanobacterial and eukaryotic pseudoparalogs were lost in evolution, or the gene was acquired by non-endosymbiotic gene transfer from an unspecified α-proteobacterium and functionally replaced its cyanobacterial and eukaryotic counterparts.

Biology Centre CAS Institute of Parasitology Branišovská 31 370 05 České Budějovice Czech Republic

Faculty of Science University of South Bohemia Branišovská 31 370 05 České Budějovice Czech Republic

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Kořený L., Sobotka R., Kovářová J., Gnipová A., Flegontov P., Horváth A., Oborník M., Ayala J.F., Lukeš J. Aerobic kinetoplastid flagellate Phytomonas does not require heme for viability. Proc. Natl. Acad. Sci. USA. 2012;109:3808–3813. doi: 10.1073/pnas.1201089109. PubMed DOI PMC

Oborník M., Green B.R. Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes. Mol. Biol. Evol. 2005;22:2343–2353. doi: 10.1093/molbev/msi230. PubMed DOI

Kořený L., Oborník M. Sequence evidence for the presence of two tetrapyrrole pathways in Euglena gracilis. Genome Biol. Evol. 2011;3:359–364. doi: 10.1093/gbe/evr029. PubMed DOI PMC

Cihlář J., Füssy Z., Horák A., Oborník M. Evolution of the tetrapyrrole biosynthetic pathway in secondary algae: Conservation, redundancy and replacement. PLoS ONE. 2016;11:e0166338. doi: 10.1371/journal.pone.0166338. PubMed DOI PMC

Cihlář J., Füssy Z., Oborník M. Evolution of tetrapyrrole pathway in eukaryotic phototrophs. Adv. Bot. Res. 2018;90:273–309.

Matsuo E., Inagaki Y. Patterns in evolutionary origins of heme, chlorophyll a and isopentenyl diphosphate biosynthetic pathways suggest non-photosynthetic periods prior to plastid replacements in dinoflagellates. PeerJ. 2018;6:e5345. doi: 10.7717/peerj.5345. PubMed DOI PMC

Kořený L., Oborník M., Lukeš J. Make it, take it, or leave it: Heme metabolism of parasites. PLoS Pathog. 2013;9:e1003088. doi: 10.1371/journal.ppat.1003088. PubMed DOI PMC

Kořený L., Sobotka R., Janouškovec J., Keeling P.J., Oborník M. Tetrapyrrole synthesis of photosynthetic chromerids is likely homologous to the unusual pathway of apicomplexan parasites. Plant Cell. 2011;23:3454–3462. doi: 10.1105/tpc.111.089102. PubMed DOI PMC

Janouškovec J., Tikhonenkov D.V., Burki F., Howe A.T., Kolísko M., Mylnikov A.P., Keeling P.J. Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives. Proc. Natl. Acad. Sci. USA. 2015;112:10200–10207. doi: 10.1073/pnas.1423790112. PubMed DOI PMC

Gawryluk R.M.R., Tikhonenkov D.V., Hehenberger E., Husník F., Mylnikov A.P., Keeling P.J. Non-photosynthetic predators are sister to red algae. Nature. 2019;572:240. doi: 10.1038/s41586-019-1398-6. PubMed DOI

Edgar R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1793. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Gouy M., Guindon S., Gascuel O. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 2010;27:221–224. doi: 10.1093/molbev/msp259. PubMed DOI

Hall T.A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999;41:95–98.

Keane T.M., Creevey C.J., Pentony M.M., Naughton T.J., McInerney J.O. Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol. Biol. 2006;6:29. doi: 10.1186/1471-2148-6-29. PubMed DOI PMC

Stamatakis A. RAxML v8.2.X Manual. Heidelberg Institute of Teoretical Studies; Heidelberg, Germany: 2016.

Lartillot N., Rodrigue N., Stubs D., Richer J. PhyloBayes 3: A Bayesian software package for phylogenetic reconstruction and molecular dating. Syst. Biol. 2013;62:611–615. doi: 10.1093/sysbio/syt022. PubMed DOI

Muñoz-Gómez S., Hess S., Burger G., Lang B.F., Susko E., Slamovits C.H., Roger A.J. An updated phylogeny of the Alphaproteobacteria reveals that the parasitic Rickettsiales and Holosporales have independent origins. eLife. 2019;8:e42535. doi: 10.7554/eLife.42535. PubMed DOI PMC

Zaremba-Niedzwiedzka K., Caceres E.F., Saw J.H., Bäckström D., Juzokaite L., Vancaester E., Seitz K.W., Anantharaman K., Starnawski P., Kjelsden K.U., et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature. 2017;541:353–358. doi: 10.1038/nature21031. PubMed DOI

Storbeck S., Rolfes S., Raux-Deery E., Warren M.J., Jahn D., Layer G. A novel pathway for the biosynthesis of heme in Archaea: Genome-based bioinformatic predictions and experinmental evidence. Archaea. 2010;2010:175050. PubMed PMC

Sato T., Haruyuki A. Novel metabolic pathways in Archaea. Curr. Opin. Microbiol. 2011;14:307–314. doi: 10.1016/j.mib.2011.04.014. PubMed DOI

Andersson A.G., Zomorodipour A., Andersson J.O., Sicheritz-Pontén T., Alsmark U.C., Powodski R.M., Näslund A.K., Eriksson A.S., Winkler H.H., Kurland C.G. The genome of Rickettsia prowazekii and the origin of mitochondria. Nature. 1998;369:133–140. doi: 10.1038/24094. PubMed DOI

Fitzpatrick D.A., Creevey C.J., McInerney J.O. Genome phylogenies indicate a meaningful α-proteobacterial phylogeny and support a grouping of the mitochondria with the Rickettsiales. Mol. Biol. Evol. 2006;23:74–85. doi: 10.1093/molbev/msj009. PubMed DOI

Williams K.P., Sobral B.W., Dickerman A.W. A robust species tree for Alphaproteobacteria. J. Bacteriol. 2007;189:4578–4586. doi: 10.1128/JB.00269-07. PubMed DOI PMC

Gray M.W. Mitochondrial evolution. Cold Spring Harb. Persp. Biol. 2012;4:a011403. doi: 10.1101/cshperspect.a011403. PubMed DOI PMC

Wang Z., Wu M. An integrated phylogenomic approach toward pinpointing the origin of mitochondria. Sci. Rep. 2015;5:7949. doi: 10.1038/srep07949. PubMed DOI PMC

Roger A.J., Muñoz-Gómez S., Kamikawa R. The origin and diversification of mitochondria. Curr. Biol. 2017;27:R1177–R1192. doi: 10.1016/j.cub.2017.09.015. PubMed DOI

Atteia A., Adrait A., Brugière S., Tardif M., van Lis R., Deusch O., Dagan T., Kuth L., Gontero B., Martin W., et al. A proteomic survey of Chlamydomonas reinhardtii mitochondria sheds light on the metabolic plasticity of the organelle and on the nature of the α-proteobacterial mitochondrial ancestor. Mol. Biol. Evol. 2009;26:1533–1548. doi: 10.1093/molbev/msp068. PubMed DOI

Esser C., Ahmadinejad N., Wiegand C., Rotte C., Sebastiani F., Gelius-Dietrich G., Henze K., Kretschmann E., Richly E., Leiser D., et al. A genome phylogeny of mitochondria among α-proteobacteria and a predominantly eubacterial ancestry of yeasts nuclear genes. Mol. Biol. Evol. 2004;21:1643–1660. doi: 10.1093/molbev/msh160. PubMed DOI

Abhishek A., Bavishi A., Bavishi A., Choudhary M. Bacterial genome chimaerism and the origin of mitochondria. Can. J. Microbiol. 2011;57:49–61. doi: 10.1139/W10-099. PubMed DOI

Carvalho D.S., Andrade R.F.S., Pihno S.T.R., Góes-Neto A., Lobãlo T.C.P., Bomfim G.C., El-Hani C.N. What are the evolutionary origins of mitochondria? A complex network approach. PLoS ONE. 2015;10:e0134988. doi: 10.1371/journal.pone.0134988. PubMed DOI PMC

Martijn J., Vosseberg J., Guy L., Offre P., Etterna T.J.G. Deep mitochondrial origin outside the sampled alphaproteobacterial. Nature. 2018;557:101–105. doi: 10.1038/s41586-018-0059-5. PubMed DOI

Dawkins R. The Selfish Gene. Oxford University Press; Oxford, UK: 1976.

Sobotka R., McLean S., Zuberova M., Hunter C.N., Tichy M. The C-terminal extension of ferrochelatase is critical for enzyme activity and for functioning of the tetrapyrrole pathway in Synechocystis strain PCC 6803. J. Bacteriol. 2008;190:2086–2095. doi: 10.1128/JB.01678-07. PubMed DOI PMC

Pazderník M., Mareš J., Pilný J., Sobotka R. The anthena-like domain of the cyanobacterial ferrochelatase can bind chlorophyll and carotenoids in an energy-dissipative configuration Binding of pigments on the ferrochelatase CAB domain. J. Biol. Chem. 2019;294:11131–11143. doi: 10.1074/jbc.RA119.008434. PubMed DOI PMC