Evolution of the Tetrapyrrole Biosynthetic Pathway in Secondary Algae: Conservation, Redundancy and Replacement

PLoS One. 2016 Nov 18;11(11):e0166338. doi: 10.1371/journal.pone.0166338. eCollection 2016.

Abstract

Tetrapyrroles such as chlorophyll and heme are indispensable for life because they are involved in energy fixation and consumption, i.e. photosynthesis and oxidative phosphorylation. In eukaryotes, the tetrapyrrole biosynthetic pathway is shaped by past endosymbioses. We investigated the origins and predicted locations of the enzymes of the heme pathway in the chlorarachniophyte Bigelowiella natans, the cryptophyte Guillardia theta, the "green" dinoflagellate Lepidodinium chlorophorum, and three dinoflagellates with diatom endosymbionts ("dinotoms"): Durinskia baltica, Glenodinium foliaceum and Kryptoperidinium foliaceum. Bigelowiella natans appears to contain two separate heme pathways analogous to those found in Euglena gracilis; one is predicted to be mitochondrial-cytosolic, while the second is predicted to be plastid-located. In the remaining algae, only plastid-type tetrapyrrole synthesis is present, with a single remnant of the mitochondrial-cytosolic pathway, a ferrochelatase of G. theta putatively located in the mitochondrion. The green dinoflagellate contains a single pathway composed of mostly rhodophyte-origin enzymes, and the dinotoms hold two heme pathways of apparently plastidal origin. We suggest that heme pathway enzymes in B. natans and L. chlorophorum share a predominantly rhodophytic origin. This implies the ancient presence of a rhodophyte-derived plastid in the chlorarachniophyte alga, analogous to the green dinoflagellate, or an exceptionally massive horizontal gene transfer.

MeSH terms

  • Biological Evolution*
  • Biosynthetic Pathways* / genetics
  • Cryptophyta / classification
  • Cryptophyta / genetics
  • Cryptophyta / metabolism*
  • Diatoms / classification
  • Diatoms / genetics
  • Diatoms / metabolism*
  • Dinoflagellida / classification
  • Dinoflagellida / genetics
  • Dinoflagellida / metabolism*
  • Gene Expression Profiling
  • Heme / metabolism
  • Phylogeny
  • Porphobilinogen Synthase / genetics
  • Porphobilinogen Synthase / metabolism
  • Tetrapyrroles / metabolism*

Substances

  • Tetrapyrroles
  • Heme
  • Porphobilinogen Synthase

Grants and funding

The Czech Science Foundation (GAP506/12/1522) and the Czech Academy of Sciences provided funding to MO and ZF. Computation resources were provided by CERIT-SC and MetaCentrum, Brno, Czech Republic. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.