Bacteria known as BALOs (Bdellovibrio-and-like organisms) are intracellular parasites that prey on other bacteria. Recent research shows that their ecological role in bacterial mortality has been underestimated, with possible implications for our understanding of ocean nutrient cycles. Other recent work shows that BALOs may have applications in ensuring seafood safety.
BALOs are intraperiplasmic parasites of other bacteria. Many planktonic eukaryotic microbes (protists) are predators, ingesting other smaller microbes, including bacteria (see previous post). Bacteria are inherently incapable of ingesting other bacteria because of the nature of their cell envelope, but the BALOs have the unusual property of preying on other Gram-negative bacteria. BALOs are widely distributed in aquatic environments, and different species and strains target particular hosts. The life cycle of the first-discovered species Bdellovibrio bacteriovorans has been extensively studied in the laboratory. Free-living cells swim at high speed and use a chemosensory system to detect high concentrations of their prey to which they attach by retractable fibres. A cocktail of enzymes creates an opening in the cell wall through which Bdellovibrio enters the periplasmic space between the outer and inner membranes, where it replicates, producing extracellular enzymes to liberate nutrients for growth. The cytoplasm of the prey is consumed and the Bdellovibrio cell elongates into a large filamentous cell. When all the nutrients are exhausted, the filament differentiates into about 15 motile cells, which then seek out new hosts after digestion of the host cell. New insights are becoming possible by the application of cryo-electron tomography to study the lifecycle in a near native state (Kaplan et al. 2022).
Credit: Bratanis et al. (2020) CC-BY-4.0.
Role of BALOs in predation of marine bacteria. BALOs) are very widespread in aquatic environments and may exert top-down control of populations of other bacteria, similar to infection by viruses (bacteriophages) although their full ecological role in food webs remains unclear. Williams et al. (2015) showed that addition of the marine BALO Halobacteriovorax spp. to seawater containing its host Vibrio parahaemolyticus led to rapid increases in the numbers of the predator, leading to death of the host bacteria. In these experiments, the viral population remained in a near steady state and no significant reduction of the vibrio prey due to bacteriophage infection was observed. This supports earlier findings that small populations of BALOs can increase rapidly in response to large numbers of prey. Williams et al. therefore concluded that Halobacteriovorax predation may be a more important cause of bacterial mortality than lysis by bacteriophages under certain environmental conditions . In later studies by this group, Chen et al. (2018) showed that Halobacteriovorax increased 18-fold, leading to rapid 104-fold reduction of Vibrio vulnificus, whereas the bacteriophage population showed no significant increase. Further experiments showed that low-nutrient conditions favoured predation and replication of Halobacteriovorax, whereas high-nutrient levels enhanced mortality by phages. This makes it likely that BALOs may have a bigger impact on bacterial mortality in natural bodies of water, which typically have low nutrient concentrations. The authors suggest that these findings may necessitate some modification of our understanding of nutrient cycling in ocean food webs. When phages lyse their bacterial hosts, membrane fragments and cellular contents are released to the dissolved organic material DOM pool, from which they can be assimilated by other microbes (the microbial loop; see diagram in previous post). But when BALOs prey on their hosts, they consume most of the cellular components before causing host cell lysis and releasing progeny bacteria. Thus, more nutrients will be retained within the particulate (POM) fraction. However, it is important to note that the experimental observations on the relative effects on mortality of phages and marine BALOs have so far only involved vibrios, which are large copiotrophic, fast-growing bacteria. It seems rather unlikely that the very small oligotrophic, slow-growing bacteria that dominate open ocean habitats can act as hosts for BALOs. Investigating this phenomenon in the natural environment would be very difficult, not least because most of these bacteria have not been cultured. To add another layer to the complexity, it is possible that BALOs are susceptible to attack by their own phages during the attack phase outside of their hosts. Indeed, phages that infect non-predatory laboratory mutants of Bdellovibrio have been described (Roberts et al. 1987; Brentlinger et al. 2002), but there do not appear to be any reports of phages infecting natural populations of BALOs. Again, this would be extremely difficult to study.
Halobacteriovorax as a biocontrol agent. Building on the successful application of phages in the food industry (Vikram et al. 2022), BALOs are now being studied for their potential use as biocontrol agents to reduce pathogens in foodstuffs (Mun et al. 2023). Halobacteriovorax has been investigated for its ability to reduce contamination by Vibrio parahaemolyticus, which is the leading cause of gastroenteritis associated with the consumption of raw or incompletely cooked seafood. High numbers of V. parahemolyticus can usually be recovered from harvested molluskan shellfish, shrimp, and crabs, especially those from estuarine and coastal waters. However, only a small number of isolates contain the virulence factors that make the bacteria pathogenic and there is considerable genome sequence variation among environmental and clinically associated strains. Virulence factors include toxins (haemolysins), iron-sequestering mechanisms, and secretion systems. Richards et al. (2023) tested the ability of four strains of Halobacteriovorax to kill 23 well-characterized and clinically relevant V. parahaemolyticus isolates obtained from diverse locations in the USA. Significant predation and killing was observed in almost all the interactions, irrespective of the geographical origin of either predator or prey. Pandemic strains of V. parahaemolyticus, which are the most common problems for seafood safety, were susceptible. These results look promising for the possibility of using BALOs as a method for depuration of seafood during processing, without affecting the texture and taste of the product.
References
Bratanis E et al. (2020). Biotechnological Potential of Bdellovibrio and Like Organisms and Their Secreted Enzymes. Front Microbiol 11: 508619.
Brentlinger KL et al. (2002) Microviridae, a family divided: Isolation, characterization, and genome sequence of φMH2K, a bacteriophage of the obligate intracellular parasitic bacterium Bdellovibrio bacteriovorus. J Bacteriol 184:1089–94.
Chen H et al. 2018) Relative Contributions of Halobacteriovorax and Bacteriophage to Bacterial Cell Death under Various Environmental Conditions. mBio 9:e01202-18.
Kaplan M et al. (2022) Dynamic structural adaptations enable the endobiotic predation of Bdellovibrio bacteriovorus. bioRxiv 2022.06.13.496000.
Mun W et al. (2023) Predatory bacteria as potential biofilm control and eradication agents in the food industry. Food Sci Biotech 1:1–15.
Richards GP et al. (2023) Predator-Prey Interactions between Halobacteriovorax and Pathogenic Vibrio parahaemolyticus Strains: Geographical Considerations and Influence of Vibrio Hemolysins. Microbiol Spectrum 10.1128/SPECTRUM.02353-23.,
Roberts RC et al. (1987) Characterization of Bdellovibrio bacteriovorus bacteriophage MAC-1. J Gen Microbiol 133:3065–70.
Vikram A et al. (2022) Phage biocontrol for reducing bacterial foodborne pathogens in produce and other foods. Curr Opin Biotechnol 78:102805.
Williams HN et al. (2016) Halobacteriovorax, an underestimated predator on bacteria: potential impact relative to viruses on bacterial mortality. ISME J 10:491–9.
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