Identification of Shemin pathway genes for tetrapyrrole biosynthesis in bacteriophage sequences from aquatic environments

Helen Wegner, Sheila Roitman, Anne Kupczok, Vanessa Braun, Jason Nicholas Woodhouse, Hans-Peter Grossart, Susanne Zehner, Oded Béjà and Nicole Frankenberg-Dinkel ()
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Helen Wegner: University of Kaiserslautern-Landau
Sheila Roitman: Technion-Israel Institute of Technology
Anne Kupczok: Wageningen University & Research
Vanessa Braun: University of Kaiserslautern-Landau
Jason Nicholas Woodhouse: Leibniz Institute of Freshwater Ecology and Inland Fisheries
Hans-Peter Grossart: Leibniz Institute of Freshwater Ecology and Inland Fisheries
Susanne Zehner: University of Kaiserslautern-Landau
Oded Béjà: Technion-Israel Institute of Technology
Nicole Frankenberg-Dinkel: University of Kaiserslautern-Landau

Nature Communications, 2024, vol. 15, issue 1, 1-11

Abstract: Abstract Tetrapyrroles such as heme, chlorophyll, and vitamin B12 are essential for various metabolic pathways. They derive from 5-aminolevulinic acid (5-ALA), which can be synthesized by a single enzyme (5-ALA synthase or AlaS, Shemin pathway) or by a two-enzyme pathway. The genomes of some bacteriophages from aquatic environments carry various tetrapyrrole biosynthesis genes. Here, we analyze available metagenomic datasets and identify alaS homologs (viral alaS, or valaS) in sequences corresponding to marine and freshwater phages. The genes are found individually or as part of complete or truncated three-gene loci encoding heme-catabolizing enzymes. Amino-acid sequence alignments and three-dimensional structure prediction support that the valaS sequences likely encode functional enzymes. Indeed, we demonstrate that is the case for a freshwater phage valaS sequence, as it can complement an Escherichia coli 5-ALA auxotroph, and an E. coli strain overexpressing the gene converts the typical AlaS substrates glycine and succinyl-CoA into 5-ALA. Thus, our work identifies valaS as an auxiliary metabolic gene in phage sequences from aquatic environments, further supporting the importance of tetrapyrrole metabolism in bacteriophage biology.

Date: 2024
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DOI: 10.1038/s41467-024-52726-3

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