Metabolism of periplasmic membrane-derived oligosaccharides by the predatory bacterium Bdellovibrio bacteriovorus 109J

Abstract

Membrane-derived oligosaccharides (MDO), a class of osmotically active carbohydrates, are the major organic solutes present in the periplasm of Escherichia coli and many other gram-negative bacteria when cells are grown in a medium of low osmolarity. Analyses of growing cells of Bdellovibnro bacteriovorus, a gram-negative predator of other bacteria, have confirmned that they also synthesize a characteristic MDO-like class of oligosaccharides. The natural growth environment of bdellovibrios is the periplasm of other gram-negative bacteria. Because of this location, prey cell MDO constitute a potential source of organic nutrients for growing bdellovibrios. Using cells of E. coli whose MDO were 3H labeled, we examined the extent to which B. bacteriovorus 109J metabolizes these prey cell components. Interestingly, there was neither significant degradation nor incorporation of prey cell MDO by bdellovibrios during the course of their intracellular growth. In fact, bdellovibrios had little capability either to degrade extracellular MDO that was made available to them or to transport glucose, the major monomeric constituent of prey cell MDO. Instead, periplasmic MDO were irreversibly lost to the extracellular environment during the period of bdellovibrio attack and penetration. Thus, although prey cell periplasmic proteins are retained, other important periplasmic components are released early in the bdellovibrio growth cycle. The loss of these MDO may aid in the destabilization of the prey cell plasma membrane, increasing the availability of cytoplasmic constituents to the periplasmic bdellovibrio.

Formation of Stable Bdelloplasts as a Starvation-Survival Strategy of Marine Bdellovibrios

“…Many different kinds of substances that are present in mixed Bdellovibrio-prey cultures, particularly if they have been established in a complex medium, are candidates for the unknown factors which induce the rupture of bdelloplasts. These substances may be released from the bdelloplasts themselves or from nonattacked prey cells and include such materials as membrane-derived oligosaccharides (12). Moreover, our results show that, depending on the phase of prey cell growth, even a protein like the enzyme alkaline phosphatase can be released from prey cells after Bdellovibrio attack.…”

Impact of bdellovibrio-and-like organisms (BALOs) on mixed species biofilm communities

“…The mechanism for entry remains unclear, however, it was proposed that, upon prey infection, the surrounding liquid would enter the infected prey, causing differential expansion or swelling of the prey cytoplasm and cell wall, which would cause their separation. During this process, the BALOs cell, which has already attached to the cytoplasmic membrane of prey, will be passively dragged into the periplasm, shedding the flagellum [89].…”

“…The small size of BALOs, relative to other bacterial species, enables their partial separation by differential centrifugation [89]. In brief, 20 mL of the fresh activated sludge samples were transferred into a clean 50 mL tubes (Falcon ® , Corning Inc.) and incubated at room temperature (24 -26°C) with shaking at 200 rpm overnight.…”

“…spp., Aquaspirillum serpens, Erwinia carotovora, Erwinia amylovora, E. coli, Xanthomonas oryzae have been used for isolation from soil and freshwater samples[89]. Studies comparing the prey range of model predators both of Alpha-BALOs (M. aeruginosavorus) and Delta-BALOs (B. bacteriovorus 109J) have shown that these two predators both were capable of attacking bacteria from the genera Acinetobacter, Aeromonas, Escherichia, Klebsiella, Pseudomonas and Vibrio, etc [162]…”

“…Both of the predators formed plaques on lawns of K. pneumoniae and P. protegens Pf-5, suggesting that the isolated predators might have prey ranges that extend across multiple bacterial species. The plaques formed by 'BALOs #2' were also consistent with those formed by relatively well-studied Bdellovibrio spp., such as B.bacteriovorus HD100 and B. bacteriovorus 109J[89,91], suggesting 'BALOs #2' is closely related to the group of Bdellovibrio spp.FISH and 16S rRNA gene sequence analysis was performed to determine the phylogenetic classification and the identities of these predatory species. For the FISH They do not penetrate into the prey's inner compartments, but rather function by adhering to the prey's surface and 'sucking' the nutrients from the attached prey cell.…”