Heme auxotrophy in abundant aquatic microbial lineages

Heme, a porphyrin ring complexed with iron, is a metalloprosthetic group of numerous proteins involved in diverse metabolic and respiratory processes across all domains of life, and is thus considered essential for respiring organisms. Several microbial groups are known to lack the de novo heme bios...

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Published in:Proceedings of the National Academy of Sciences - PNAS 2021-11, Vol.118 (47), p.1-9
Main Authors: Kim, Suhyun, Kang, Ilnam, Lee, Jin-Won, Jeon, Che Ok, Giovannoni, Stephen J., Cho, Jang-Cheon
Format: Article
Language:English
Subjects:
Aquatic habitats
Archaea - genetics
Archaea - metabolism
Auxotrophy
Bacteria - genetics
Bacteria - metabolism
Biodiversity
Biological Sciences
Biosynthesis
Biosynthetic Pathways
Ecosystem
Fresh Water - microbiology
Freshwater environments
Genome, Bacterial
Genomes
Growth factors
Heme
Heme - metabolism
Microorganisms
Porphyrins
Riboflavin
Symbionts
Taxonomy
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Summary:Heme, a porphyrin ring complexed with iron, is a metalloprosthetic group of numerous proteins involved in diverse metabolic and respiratory processes across all domains of life, and is thus considered essential for respiring organisms. Several microbial groups are known to lack the de novo heme biosynthetic pathway and therefore require exogenous heme from the environment. These heme auxotroph groups are largely limited to pathogens, symbionts, or microorganisms living in nutrient-replete conditions, whereas the complete absence of heme biosynthesis is extremely rare in free-living organisms. Here, we show that the acI lineage, a predominant and ubiquitous free-living bacterial group in freshwater habitats, is auxotrophic for heme, based on the experimental or genomic evidence. We found that two recently cultivated acI isolates require exogenous heme for their growth. One of the cultured acI isolates also exhibited auxotrophy for riboflavin. According to whole-genome analyses, all (n = 20) isolated acI strains lacked essential enzymes necessary for heme biosynthesis, indicating that heme auxotrophy is a conserved trait in this lineage. Analyses of >24,000 representative genomes for species clusters of the Genome Taxonomy Database revealed that heme auxotrophy is widespread across abundant but not-yet-cultivated microbial groups, including Patescibacteria, Marinisomatota (SAR406), Actinomarinales (OM1), and Marine groups IIb and III of Euryarchaeota. Our findings indicate that heme auxotrophy is a more common phenomenon than previously thought, and may lead to use of heme as a growth factor to increase the cultured microbial diversity.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2102750118