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Monitoring the Reductive and Oxidative Half-Reactions of a Flavin-Dependent Monooxygenase using Stopped-Flow Spectrophotometry
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Origin and Evolution of Flavin-Based Electron Bifurcating Enzymes.

Saroj Poudel1, Eric C Dunham1, Melody R Lindsay1

  • 1Department of Microbiology and Immunology, Montana State University, Bozeman, MT, United States.

Frontiers in Microbiology
|August 21, 2018
PubMed
Summary

Flavin-based electron bifurcation (Bf) enzymes, crucial for anaerobic energy metabolism, evolved multiple times through flavoprotein recruitment. These enzymes enhance metabolic efficiency and energy capture in subsurface environments.

Keywords:
LUCAanoxicelectron bifurcationferredoxinflavinmetagenomesoxidoreductasesubsurface

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Area of Science:

  • Biochemistry
  • Evolutionary Biology
  • Microbial Ecology

Background:

  • Flavin-based electron bifurcation (Bf) is a metabolic strategy used by certain oxidoreductases to couple energetically unfavorable reactions.
  • Bf enzymes are vital for maintaining cellular redox balance and improving metabolic efficiency, particularly in anaerobic microorganisms.
  • A comprehensive understanding of Bf enzyme diversity and evolutionary origins is currently lacking.

Purpose of the Study:

  • To investigate the taxonomic distribution, functional diversity, and evolutionary history of Bf enzyme homologs across diverse microbial life.
  • To determine the origins and evolutionary trajectory of flavin-based electron bifurcation in prokaryotes and eukaryotes.
  • To explore the ecological relevance of Bf enzymes in different environmental niches, particularly subsurface habitats.

Main Methods:

  • Bioinformatic analysis of Bf enzyme homologs in 4,588 archaeal, bacterial, and eukaryal genomes.
  • Analysis of 3,136 community metagenomes to assess Bf enzyme prevalence in environmental samples.
  • Phylogenetic analyses of oxidoreductase catalytic subunits to reconstruct evolutionary relationships and identify recruitment events.

Main Results:

  • Bf homologs are predominantly found in anaerobic microorganisms, including sulfate-reducers, acetogens, fermenters, and methanogens.
  • Phylogenetic analyses indicate that Bf enzymes are not ancient and likely arose from multiple independent recruitments of flavoproteins to existing oxidoreductases.
  • Bf enzyme homologs are enriched in subsurface environments, with the earliest evolving homologs originating from deep subsurface habitats.

Conclusions:

  • The evolution of flavin-based electron bifurcation is a result of multiple independent recruitment events, enabling enhanced energy metabolism in anaerobes.
  • Bf enzymes play a significant role in the adaptation of microorganisms to energy-limited subsurface environments.
  • The findings highlight the importance of Bf enzymes in microbial energy capture and metabolic optimization in anoxic ecosystems.