Composition of distinct sub-proteomes in Myxococcus xanthus: metabolic cost and amino acid availability

Abstract

Subsets of proteins involved in distinct functional processes are subject to different selective pressures. We investigated whether there is an amino acid composition bias (AACB) inherent in discrete subsets of proteins, and whether we could identify changing patterns of AACB during the life cycle of the social bacterium Myxococcus xanthus. We quantitatively characterised the cellular, soluble secreted, and outer membrane vesicle (OMV) sub-proteomes of M. xanthus, identifying 315 proteins. The AACB of the cellular proteome differed only slightly from that deduced from the genome, suggesting that genome-inferred proteomes can accurately reflect the AACB of their host. Inferred AA deficiencies arising from prey consumption were exacerbated by the requirements of the 68%GC genome, whose character thus seems to be selected for directly rather than via the proteome. In our analysis, distinct subsets of the proteome (whether segregated spatially or temporally) exhibited distinct AACB, presumably tailored according to the needs of the organism's lifestyle and nutrient availability. Secreted AAs tend to be of lower cost than those retained in the cell, except for the early developmental A-signal, which is a particularly costly sub-proteome. We propose a model of AA reallocation during the M. xanthus life cycle, involving ribophagy during early starvation and sequestration of limiting AAs within cells during development.

The Predation Strategy of Myxococcus xanthus

“…xanthus OMVs has been shown to differ from that of the periplasm and outer membrane, hinting to the presence of a dedicated protein sorting mechanism to load OMVs (Kahnt et al, 2010;Evans et al, 2012;Berleman et al, 2014;Whitworth et al, 2015). OMVs contain several proteins with predicted hydrolytic functions, as well as antibiotics, such as myxovirescin A and the antifungal myxalamide (Kahnt et al, 2010;Evans et al, 2012;Berleman et al, 2014).…”

Is “Wolf‐Pack” Predation by Antimicrobial Bacteria Cooperative? Cell Behaviour and Predatory Mechanisms Indicate Profound Selfishness, Even when Working Alongside Kin

“…The foraging of bees is synergistic because signaling between individuals enhances each individual's ability to locate food. Myxobacteria have an extensive repertoire of signaling proteins . They respond to molecules secreted by some prey, and motility‐based behavioral changes have been observed during predation .…”

“…Myxobacteria have an extensive repertoire of signaling proteins. [14,21] They respond to molecules secreted by some prey, and motility-based behavioral changes have been observed during predation. [66,67] Nevertheless, virtually no transcriptional changes were observed in the predator when exposed to prey Escherichia coli (E. coli), [68] precluding cell-cell signaling dependent stimulation of predatory gene expression.…”

“…It is known that myxobacteria secrete enzymes with antibacterial activity, [11] and that the outer membrane vesicles (OMVs) they secrete are also intrinsically antimicrobial. [12] However, even though they have low-complexity proteomes, [13,14] we largely do not know which OMV cargo proteins are responsible for killing a particular prey, nor (except in a few specific cases) can we explain why a particular prey is more or less susceptible to communal attack by myxobacteria. [15][16][17][18] In contrast, we know considerably more about the molecular mechanisms and evolutionary forces at play during fruiting body formation, a cooperative process that myxobacteria engage in when prey is scarce.…”

The “hole” story of predatory outer-membrane vesicles

“…Regarding the PG-lytic enzymes, Evans et al (2012) identified PG-specific amidases and lysozyme within the OMVs released by this predator. Yet 2 separate high-throughput proteomic studies of these OMVs resulted in the identification of only a single N-acetylmuramoyl-L-alanine amidase (Kahn et al 2013;Berleman et al 2014); no autolysin was identified in a third, and most recent, study (Whitworth et al 2015). Again, it is possible that the annotations of the databases are incomplete or incorrect to preclude complete identification of the OMV proteomes.…”