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The Effect of Visible Light on Cell Envelope Subproteome during Vibrio harveyi Survival at 20 °C in Seawater.

ABSTRACT: A number of Vibrio spp. belong to the well-studied model organisms used to understand the strategies developed by marine bacteria to cope with adverse conditions (starvation, suboptimal temperature, solar radiation, etc.) in their natural environments. Temperature and nutrient availability are considered to be the key factors that influence Vibrio harveyi physiology, morphology, and persistence in aquatic systems. In contrast to the well-studied effects of temperature and starvation on Vibrio survival, little is known about the impact of visible light able to cause photooxidative stress. Here we employ V. harveyi ATCC 14126^T as a model organism to analyze and compare the survival patterns and changes in the protein composition of its cell envelope during the long-term permanence of this bacterium in seawater microcosm at 20 °C in the presence and absence of illumination with visible light. We found that V. harveyi exposure to visible light reduces cell culturability likely inducing the entry into the Viable but Non Culturable state (VBNC), whereas populations maintained in darkness remained culturable for at least 21 days. Despite these differences, the starved cells in both populations underwent morphological changes by reducing their size. Moreover, further proteomic analysis revealed a number of changes in the composition of cell envelope potentially accountable for the different adaptation pattern manifested in the absence and presence of visible light.

SUBMITTER: Orruno M

PROVIDER: S-EPMC8001661 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Bacteria coping with oxygen deficiency use alternative terminal electron acceptors for NADH regeneration, particularly fumarate. Fumarate is reduced by the FAD_binding_2 domain of cytoplasmic fumarate reductase in many bacteria. The variability of the primary structure of this domain in homologous proteins suggests the existence of reducing activities with different specificities. Here, we produced and characterized one such protein encoded in the Vibrio harveyi genome (GenBank ID: AIV07243) and found it to be a specific NADH:acrylate oxidoreductase (ARD). This previously unknown enzyme is formed by the OYE-like, FMN_bind, and FAD_binding_2 domains and contains covalently bound flavin mononucleotide (FMN) and noncovalently bound flavin adenine dinucleotide (FAD) and FMN in a ratio of 1:1:1. The covalently bound FMN is absolutely required for activity and is attached by the specific flavin transferase, ApbE, to the FMN_bind domain. Quantitative reverse transcription PCR (RT-qPCR) and activity measurements indicated dramatic stimulation of ARD biosynthesis by acrylate in the V. harveyi cells grown aerobically. In contrast, the ard gene expression in the cells grown anaerobically without acrylate was higher than that in aerobic cultures and increased only 2-fold in the presence of acrylate. These findings suggest that the principal role of ARD in Vibrio is energy-saving detoxification of acrylate coming from the environment. IMPORTANCE The benefits of the massive genomic information accumulated in recent years for biological sciences have been limited by the lack of data on the function of most gene products. Approximately half of the known prokaryotic genes are annotated as "proteins with unknown functions," and many other genes are annotated incorrectly. Thus, the functional and structural characterization of the products of such genes, including identification of all existing enzymatic activities, is a pressing issue in modern biochemistry. In this work, we have shown that the product of the V. harveyi ard gene exhibits a yet-undescribed NADH:acrylate oxidoreductase activity. This activity may allow acrylate detoxification and its use as a terminal electron acceptor in anaerobic or substrate in aerobic respiration of marine and other bacteria.

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The Effect of Visible Light on Cell Envelope Subproteome during Vibrio harveyi Survival at 20 °C in Seawater.

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