Independently evolved extracellular electron transfer pathways in ecologically diverse Desulfobacterota

Area of Science:

• Microbiology
• Biochemistry
• Environmental Science

Background:

• Extracellular electron transfer (EET) is crucial for biogeochemical cycles and biotechnological applications.
• Key EET pathways include metal-reducing (Mtr), outer-membrane cytochrome (Omc), and porin-cytochrome (Pcc), which are phylogenetically distinct.
• These pathways facilitate electron transfer to insoluble electron acceptors via trans-outer membrane cytochrome complexes.

Purpose of the Study:

• To investigate the extracellular electron transfer mechanisms in the high-current producing bacterium Desulfuromonas acetexigens.
• To explore the co-expression of Mtr, Omc, and Pcc pathways in Desulfobacterota species.
• To identify novel metal-reducing proteins and assess the diversity of EET pathways in diverse ecological environments.

Main Methods:

• Differential transcript and protein level analysis of Mtr, Omc, and Pcc pathways in D. acetexigens under EET conditions.
• Bioinformatic analysis of over 40 Desulfobacterota species to identify EET pathway genes.
• Phylogenetic analysis of newly identified metal-reducing proteins.

Main Results:

• Desulfuromonas acetexigens differentially co-expresses Mtr, Omc, and Pcc pathways along with high-molecular-weight cytochromes (up to 86 hemes) under EET conditions.
• Over 40 Desulfobacterota species were found to encode Omc and Mtr pathways, with most also expressing the Pcc pathway.
• A major lineage of novel metal-reducing proteins was identified in Desulfobacterota, expanding known protein diversity.
• mtrCAB genes were not found in Desulfobacterota, and simultaneous expression of these distant pathways was previously unreported.

Conclusions:

• Extracellular electron transfer pathways are more widespread across microbial taxa than previously believed.
• The simultaneous expression of phylogenetically distant EET pathways in D. acetexigens highlights microbial versatility.
• These findings have significant ecological implications and reveal new opportunities for biotechnological applications.