Marinobacter atlanticus electrode biofilms differentially regulate gene expression depending on electrode potential and lifestyle

Abstract

Marinobacter spp. are opportunitrophs with a broad metabolic range including interactions with metals and electrodes. Marinobacter atlanticus strain CP1 was previously isolated from a cathode biofilm microbial community enriched from a sediment microbial fuel cell. Like other Marinobacter spp., M. atlanticus generates small amounts of electrical current when grown as a biofilm on an electrode, which is enhanced by the addition of redox mediators. However, the molecular mechanism resulting in extracellular electron transfer is unknown. Here, RNA-sequencing was used to determine changes in gene expression in electrode-attached and planktonic cells of M. atlanticus when grown at electrode potentials that enable current production (310 and 510 mV vs. SHE) compared to a potential that enables electron uptake (160 mV). Cells grown at current-producing potentials had increased expression of genes for molybdate transport, regardless of planktonic or attached lifestyle. Electrode-attached cells at current-producing potentials showed increased expression of the major export protein for the type VI secretion system. Growth at 160 mV resulted in an increase in expression of genes related to stress response and DNA repair including both RecBCD and the LexA/RecA regulatory network, as well as genes for copper homeostasis. Changes in expression of proteins with PEP C-terminal extracellular export motifs suggests that M. atlanticus is remodeling the biofilm matrix in response to electrode potential. These results improve our understanding of the physiological adaptations required for M. atlanticus growth on electrodes, and suggest a role for metal acquisition, either as a requirement for metal cofactors of redox proteins or as a possible electron shuttling mechanism.

Conservation of Energetic Pathways for Electroautotrophy in the Uncultivated Candidate Order Tenderiales

“…Five orthogroups were found which contained adhesion related histidine kinase or diguanylate-cyclase domains. These could regulate attachment as found in other electroactive biofilms (35,36).…”

Species-specific responses of marine bacteria to environmental perturbation

“…Previous studies either provide support against [ 37 , 40 ] or, interestingly, in favor of [ 41 , 42 , 75 ] the perception of Marinobacter as an opportunitroph. Our transcriptomic datasets and CA-Metatranscriptomic analysis show different expression responses across the metabolic map and suggest very different responses in a specialist-vs-opportunistic framework between Marinobacter and Colwellia (Fig.…”

Bacteria Associated With Phaeocystis globosa and Their Influence on Colony Formation

“…GS7 significantly impaired the growth and colony formation of P. globosa . The inhibition effect on P. globosa growth might be related to the physiological change of Marinobacter cells at high cell densities compared to low cell densities, such as chemotaxis, cell motility, and attachment ( Sonnenschein Eva et al, 2012 ), or extracellular electron transfer ( Eddie et al, 2021 ), or discharging of chemical mediators such as antibacterial and algicidal compounds ( Imai et al, 1993 ; Mayali and Azam, 2004 ; Meyer et al, 2017 ; Cirri and Pohnert, 2019 ). Lifestyle change of Alteromonas , another opportunitroph frequently associated with marine phytoplankton, has been observed when co-culturing with Trichodesmium ( Hou et al, 2018 ).…”