Adaptation of Vibrio cholerae to Hypoxic Environments

Abstract

Bacteria can colonize virtually any environment on Earth due to their remarkable capacity to detect and respond quickly and adequately to environmental stressors. Vibrio cholerae is a cosmopolitan bacterium that inhabits a vast range of environments. The V. cholerae life cycle comprises diverse environmental and infective stages. The bacterium is found in aquatic ecosystems both under free-living conditions or associated with a wide range of aquatic organisms, and some strains are also capable of causing epidemics in humans. In order to adapt between environments, V. cholerae possesses a versatile metabolism characterized by the rapid cross-regulation of energy-producing pathways. Low oxygen concentration is a key environmental factor that governs V. cholerae physiology. This article reviews the metabolic plasticity that enables V. cholerae to thrive on low oxygen concentrations and its role in environmental and host adaptation.

Keywords: TMAO; Vibrio cholerae; enteropathogen; fermentation; fitness; fumarate; nitrate; respiration.

FIGURE 1

Schematic of redox balance and energy generating pathways in V. cholerae during (A) oxic growth, where V. cholerae obtains ATP through oxidative phosphorylation by respiration of oxygen using an electron transport chain initiated by a Na⁺-translocating NADH:quinone oxidoreductase (Na⁺-NQR), (B) hypoxic growth, where V. cholerae obtains energy by fermentation. In this condition, ATP is generated by substrate-level phosphorylation. As in the absence of final electron acceptors respiration is inhibited, the proton motive force (PMF) is established by proton pumping by the ATPase (with ATP consumption), and by sodium transporters (C) hypoxic growth in the presence of AEA, where V. cholerae is able to simultaneously obtain energy by substrate-level phosphorylation during fermentation and respiration of AEA. Represented in each scheme are only components experimentally demonstrated as relevant for the growth of the bacteria. Other components of the respiratory chain, such as alternative NADH dehydrogenases (see Table 1) whose inactivation does not affect V. cholerae growth are not shown.

FIGURE 2

Schematic representations of V. cholerae niches where oxygen concentrations are limited. (A) Within the biofilm bacteria faces different oxygen concentrations. Cells situated in the periphery of the biofilm, where oxygen tensions are higher, will obtain energy through respiration of oxygen. However, cells situated in inner layers, where oxygen concentrations are scarce, will obtain energy through fermentation or/and nitrate, TMAO, fumarate respiration. (B) Human intestine colonization model showing the divergent outcomes during anaerobic nitrate respiration on bacterial expansion dependent on oxygen concentrations and pH. Pyr: pyruvate. Ferm: fermentative products. Fum: fumarate. Succ: succinate.