Reward for Bdellovibrio bacteriovorus for preying on a polyhydroxyalkanoate producer

Abstract

Bdellovibrio bacteriovorus HD100 is an obligate predator that invades and grows within the periplasm of Gram-negative bacteria, including mcl-polyhydroxyalkanoate (PHA) producers such as Pseudomonas putida. We investigated the impact of prey PHA content on the predator fitness and the potential advantages for preying on a PHA producer. Using a new procedure to control P. putida KT2442 cell size we demonstrated that the number of Bdellovibrio progeny depends on the prey biomass and not on the viable prey cell number or PHA content. The presence of mcl-PHA hydrolysed products in the culture supernatant after predation on P. putida KT42Z, a PHA producing strain lacking PhaZ depolymerase, confirmed the ability of Bdellovibrio to degrade the prey's PHA. Predator motility was higher when growing on PHA accumulating prey. External addition of PHA polymer (latex suspension) to Bdellovibrio preying on the PHA minus mutant P. putida KT42C1 restored predator movement, suggesting that PHA is a key prey component to sustain predator swimming speed. High velocities observed in Bdellovibrio preying on the PHA producing strain were correlated to high intracellular ATP levels of the predator. These effects brought Bdellovibrio fitness benefits as predation on PHA producers was more efficient than predation on non-producing bacteria.

A holistic view of polyhydroxyalkanoate metabolism in Pseudomonas putida

“…Thus, the number and size of the cells directly relate to the ability to accumulate PHAs. Furthermore, the cell size of the P. putida mutant unable to accumulate PHA is inversely correlated to the C/N ratio of the culture medium (Martínez et al ., ) (Fig. ).…”

“…Soil bacteria face to different and fluctuating stresses, examples of PHA impact on bacterial physiology are: A zospirillum , and other rhizosphere bacteria in keeping plant and microorganism symbiosis; the formation of spores or cysts is linked to the PHA cycle in B acillus cereus and A zotobacter vinelandii ; microbial biofilm formation in P seudomonas aeruginosa (Kadouri et al ., ; Castro‐Sowinski et al ., ); promotion of predator fitness in B . bacteriovorus (Martínez et al ., ). B, C. The synthesis of PHA granules determines the cellular size due to the control of the biomass distribution.…”

“…A highly motile delta proteobacterium, B. bacteriovorus , is ubiquitously distributed in terrestrial and aquatic environments. It grows and reproduces in the periplasm of other Gram‐negative prey bacteria, including P. putida KT2440 (Rendulic et al ., ; Martínez et al ., ). Its mcl‐PHA depolymerase (PhaZ Bd , ORF Bd3709), part of the hydrolytic arsenal needed for its predatory life cycle, shows significant amino acid sequence similarity to the prototype extracellular mcl‐PHA depolymerase PhaZ GK13 .…”

“…These findings prompted the investigation of the ability of these predators to prey upon PHA‐accumulating strains and the impact of this on their fitness (Martínez et al ., ). In P. putida and other PHA producers, PHAs play an important role in bacterial fitness, improving survival under environmental stress conditions in water and soil, and providing a means of reacting to changing carbon and energy availability conditions (Kadouri et al ., ; Zhao et al ., ).…”

Bacterial predation in a marine host-associated microbiome

“…Predation by BALOs also releases nutrients (Martínez et al, 2013), affecting biogeochemical cycling and production in nutrient-limited environments, similar to the effects of phage (Fuhrman, 1999;Brussaard et al, 2008). In contrast to viruses, which are the most abundant biological entity in the marine environment and maintain abundances approximately in an order of magnitude greater than their hosts, BALOs do not need to be in high initial concentrations in the environment to drive significant bacterial mortality of their prey (Richards et al, 2012;Williams et al, 2016).…”