Environmental Regulation of the Distribution and Ecology of Bdellovibrio and Like Organisms

Abstract

The impact of key environmental factors, salinity, prey, and temperature, on the survival and ecology of Bdellovibrio and like bacteria (BALOs), including the freshwater/terrestrial, non-halotolerant group and the halophilic Halobacteriovorax strains, has been assessed based on a review of data in the literature. These topics have been studied by numerous investigators for nearly six decades now, and much valuable information has been amassed and reported. The collective data shows that salinity, prey, and temperature play a major role in, not only the growth and survival of BALOs, but also the structure and composition of BALO communities and the distribution of the predators. Salinity is a major determinant in the selection of BALO habitats, distribution, prey bacteria, and systematics. Halophilic BALOs require salt for cellular functions and are found only in saltwater habitats, and prey primarily on saltwater bacteria. To the contrary, freshwater/terrestrial BALOs are non-halotolerant and inhibited by salt concentrations greater than 0.5%, and are restricted to freshwater, soils, and other low salt environments. They prey preferentially on bacteria in the same habitats. The halophilic BALOs are further separated on the basis of their tolerance to various salt concentrations. Some strains are found in low salt environments and others in high salt regions. In situ studies have demonstrated that salinity gradients in estuarine systems govern the type of BALO communities that will persist within a specific gradient. Bacterial prey for BALOs functions more than just being a substrate for the predators and include the potential for different prey species to structure the BALO community at the phylotype level. The pattern of susceptibility or resistance of various bacteria species has been used almost universally to differentiate strains of new BALO isolates. However, the method suffers from a lack of uniformity among different laboratories. The use of molecular methods such as comparative analysis of the 16S rDNA gene and metagenomics have provided more specific approaches to distinguished between isolates. Differences in temperature growth range among different BALO groups and strains have been demonstrated in many laboratory experiments. The temperature optima and growth range for the saltwater BALOs is typically lower than that of the freshwater/terrestrial BALOs. The collective data shows not only that environmental factors have a great impact on BALO ecology, but also how the various factors affect BALO populations in nature.

Keywords: Bdellovibrio and like organisms; Halobacteriovorax; environmental factors; predator-prey interactions; predatory bacteria; prey susceptibility.

FIGURE 1

Schematic diagram of the evolution of the nomenclature and taxonomy of Bdellovibrio-like bacteria from their discovery (Stolp and Petzold, 1962) and naming (Stolp and Starr, 1963) as Bdellovibrio bacteriovorus to 2020. Subsequently, two major groups were defined by their requirement or tolerance to sodium chloride, the halophilic or marine Bdellovibrio, and the freshwater or terrestrial variety, Bdellovibrio bacteriovorus. In the early 1970s, Bdellovibrio bacteriovorus was split, establishing two new species, Bdellovibrio. starrii and Bdellovibrio stolpii (Seidler et al., 1972). Later, the original genus, Bdellovibrio, was split into two genera, Bacteriovorax (Baer et al., 2000) and Peredibacter starrii (Davidov and Jurkevitch, 2004). Then came the reclassification of Bacteriovorax stolpii as Bacteriolyticum stolpii (Piñeiro et al., 2008), leaving the genus Bacteriovorax comprised solely of the halophilic members. To correct an error, the original name Bacteriovorax stolpii was restored, as it is the type species for the genus Bacteriovorax. The previous saltwater “Bacteriovorax” was then assigned to a new genus, Halobacteriovorax (Koval et al., 2015).

FIGURE 2

The succession of Bacteriovorax (now Halobacteriovorax) phylotypes isolated from the top and bottom water samples and sediment samples from three stations, Baltimore (oligohaline zone), East Middle (mesohaline zone), and Mouth (polyhaline zone) by season along Chesapeake Bay salinity gradient in 2005 and 2006. The percentages shown along the Y-axis are based on mean counts of Halobacteriovorax plaques from five transects of the Bay conducted in different seasons in a 2-year period over a salinity range between 5 and 31 ppt. Reprint from Piñeiro et al. (2013).

FIGURE 3

Quantitation efficiencies of various bacterial prey compared with that of V. parahaemolyticus P-5. Reprinted from Schoeffield and Williams (1990). Copyright (1990) American Society for Microbiology.