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. 2022 Mar 29:13:851738.
doi: 10.3389/fgene.2022.851738. eCollection 2022.

Origin and Evolution of Enzymes with MIO Prosthetic Group: Microbial Coevolution After the Mass Extinction Event

Fei Peng  1 , Ulrike Engel  1 , Habibu Aliyu  1 , Jens Rudat  1
Affiliations

Origin and Evolution of Enzymes with MIO Prosthetic Group: Microbial Coevolution After the Mass Extinction Event

Fei Peng et al. Front Genet. .

Abstract

After major mass extinction events, ancient plants and terrestrial vertebrates were faced with various challenges, especially ultraviolet (UV) light. These stresses probably resulted in changes in the biosynthetic pathways, which employed the MIO (3,5-dihydro-5-methylidene-4H-imidazole-4-one)-dependent enzymes (ammonia-lyase and aminomutase), leading to enhanced accumulation of metabolites for defense against UV radiation, pathogens, and microorganisms. Up to now, the origin and evolution of genes from this superfamily have not been extensively studied. In this report, we perform an analysis of the phylogenetic relations between the members of the aromatic amino acid MIO-dependent enzymes (AAM), which demonstrate that they most probably have a common evolutionary origin from ancient bacteria. In early soil environments, numerous bacterial species with tyrosine ammonia-lyase genes (TAL; EC 4.3.1.23) developed tyrosine aminomutase (TAM; EC 5.4.3.6) activity as a side reaction for competing with their neighbors in the community. These genes also evolved into other TAL-like enzymes, such as histidine ammonia-lyase (HAL, EC 4.3.1.3) and phenylalanine ammonia-lyase (PAL; EC 4.3.1.24), in different bacterial species for metabolite production and accumulation for adaptation to adverse terrestrial environmental conditions. On the other hand, the existence of phenylalanine aminomutase (PAM; EC 5.4.3.10) and phenylalanine/tyrosine ammonia-lyase (PTAL; EC 4.3.1.25) strongly indicates the horizontal gene transfer (HGT) between bacteria, fungi, and plants in symbiotic association after acquiring the PAL gene from their ancestor.

Keywords: MIO-dependent enzymes; a mass extinction event; microbial coevolution; minimal ancestor deviation; rooted phylogenetic tree.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
The proposed mechanism for the MIO in HAL and GFP formation by posttranslational modification.
FIGURE 2
FIGURE 2
Two proposals for ammonia elimination by R. toruloides PAL. The other residues help to orient and stabilize the carboxyl group of arylalanine amino acids.
FIGURE 3
FIGURE 3
The phenylpropanoid pathway in plants for the production of flavonoids and monolignols under abiotic stress conditions.
FIGURE 4
FIGURE 4
Different histidine degradation pathways. Conversion of histidine to glutamate.
FIGURE 5
FIGURE 5
Phylogenetic tree of arylalanine amino acid ammonia-lyase and aminomutase homologs retrieved from the Swissprot database. Characterized ammonia-lyases are shown in the square while characterized aminomutases are shown in the circle. The color coding corresponds to the substrates of the enzymes: histidine (yellow), phenylalanine (green), tyrosine (purple). The source organisms in the tree are color-coded in the outer ring according to their origin.
FIGURE 6
FIGURE 6
(A) Overlap X-ray crystal structures of PpHAL from Pseudomonas putida (PDB entry 1GKM, blue), RtPAL from R. toruloides (PDB entry 1T6J, yellow), and RsTAL from Rhodobacter sphaeroides (PDB entry 2O6Y, pink) (B) The inner (blue) and outer (red) loops in RsTAL from two chains. The MIO is colored in red.
See this image and copyright information in PMC

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