Novel Insights on Extracellular Electron Transfer Networks in the Desulfovibrionaceae Family: Unveiling the Potential Significance of Horizontal Gene Transfer

Author:

Gonzalez Valentina123,Abarca-Hurtado Josefina1ORCID,Arancibia Alejandra14,Claverías Fernanda2,Guevara Miguel R.5ORCID,Orellana Roberto146ORCID

Affiliation:

1. Laboratorio de Biología Celular y Ecofisiología Microbiana, Facultad de Ciencias Naturales y Exactas, Universidad de Playa Ancha, Leopoldo Carvallo 270, Valparaíso 2360001, Chile

2. Laboratorio de Microbiología Molecular y Biotecnología Ambiental, Departamento de Química & Centro de Biotecnología Daniel Alkalay-Lowitt, Universidad Técnica Federico Santa María, Avenida España 1680, Valparaíso 2390123, Chile

3. Departamento de Química y Medio Ambiente, Sede Viña del Mar, Universidad Técnica Federico Santa María, Avenida Federico Santa María 6090, Viña del Mar 2520000, Chile

4. HUB Ambiental UPLA, Universidad de Playa Ancha, Leopoldo Carvallo 207, Playa Ancha, Valparaíso 2340000, Chile

5. Laboratorio de Data Science, Facultad de Ingeniería, Universidad de Playa Ancha, Leopoldo Carvallo 270, Valparaíso 2340000, Chile

6. Núcleo Milenio BioGEM, Valparaíso 2390123, Chile

Abstract

Some sulfate-reducing bacteria (SRB), mainly belonging to the Desulfovibrionaceae family, have evolved the capability to conserve energy through microbial extracellular electron transfer (EET), suggesting that this process may be more widespread than previously believed. While previous evidence has shown that mobile genetic elements drive the plasticity and evolution of SRB and iron-reducing bacteria (FeRB), few have investigated the shared molecular mechanisms related to EET. To address this, we analyzed the prevalence and abundance of EET elements and how they contributed to their differentiation among 42 members of the Desulfovibrionaceae family and 23 and 59 members of Geobacteraceae and Shewanellaceae, respectively. Proteins involved in EET, such as the cytochromes PpcA and CymA, the outer membrane protein OmpJ, and the iron–sulfur cluster-binding CbcT, exhibited widespread distribution within Desulfovibrionaceae. Some of these showed modular diversification. Additional evidence revealed that horizontal gene transfer was involved in the acquiring and losing of critical genes, increasing the diversification and plasticity between the three families. The results suggest that specific EET genes were widely disseminated through horizontal transfer, where some changes reflected environmental adaptations. These findings enhance our comprehension of the evolution and distribution of proteins involved in EET processes, shedding light on their role in iron and sulfur biogeochemical cycling.

Funder

ANID

Fondecyt

Publisher

MDPI AG

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