Redox-based chemical warfare is a primary driver of microbial community assembly. Here, we show that the predatory bacterium Myxococcus xanthus employs a spatial division of labor between two inducible monofunctional catalases, mxKatB and mxKatE, to overcome prey-derived hydrogen peroxide (H₂O₂). Quantitative transcript analysis revealed distinct regulatory specificities: mxkatB was the dominant transcriptional responder to exogenous H₂O₂, whereas mxkatE was preferentially induced by UV irradiation. Biochemical analyses demonstrated strict compartmentalization of enzymatic activity. mxKatE functioned intracellularly, consistent with a role in mitigating endogenous genotoxic stress. In contrast, mxKatB, which harbors an N-terminal Sec-dependent signal peptide, was exclusively localized to the extracellular milieu. Targeted gene deletions corroborated these non-redundant physiological roles. ΔkatE mutant exhibited severe growth defects and heightened sensitivity to UV and H₂O₂ yet retained full predation proficiency. Conversely, ΔkatB mutant displayed unaltered vegetative fitness but were severely impaired in prey lysis due to oxidative inactivation of secreted bacteriolytic enzymes. Failure of cross-complementation confirmed that spatial localization, rather than catalytic capacity, dictates enzyme function. Our findings establish that M. xanthus deploys an extracellular catalase shield to protect its exoenzyme arsenal from prey-derived oxidants. This spatial specialization of antioxidant defenses represents a sophisticated strategy that directly determines the outcome of bacterial predation and shapes interspecies interactions within microbial communities. IMPORTANCE Predatory bacteria such as M. xanthus must withstand chemical defenses deployed by their prey. We show that M. xanthus uses a spatially specialized antioxidant system: an extracellular catalase (mxKatB) secreted to shield its lytic enzymes from prey-derived hydrogen peroxide, and an intracellular catalase (mxKatE) that handles endogenous oxidative stress. This division of labor reveals that bacterial antioxidant defenses can be compartmentalized to protect extracellular weaponry rather than the cell itself, adding a new dimension to how spatial organization of stress responses influences the outcome of microbial competition.
D. Sheng, Xuan-qi Zhang, Xin-yao Yan et al.· bioRxiv· 0 citations
ABSTRACT Peptidylprolyl isomerase (PPIase) catalyzes the rate-limiting step of proline cis-trans isomerization during protein folding. In bacteria, multiple PPIases are commonly present and participate in diverse physiological processes. Myxococcus xanthus DK1622 possesses as many as 17 PPIase genes. We previously reported the functional divergence of the four trigger factor family PPIases. Here, we systematically assessed the contributions of the remaining PPIases in cell survival, sociality, and stress tolerance. Pin1, localized in the periplasm, was essential for cell growth. Absence of the membrane-bound Pin3 impaired the social motility, predation ability, and sporulation but did not affect the fruiting body formation of M. xanthus. Furthermore, nearly all M. xanthus PPIases contributed to tolerance to environmental stresses. The transcriptional levels and expression patterns of these PPIases varied distinctly, even among members of the same family or with high sequence homology. Our findings provide a comprehensive view of functional divergences and suggest a potential functional cooperation network of PPIases in M. xanthus. IMPORTANCE Peptidylprolyl isomerase (PPIase), a ubiquitous enzyme present across nearly all kingdoms of life, catalyzes the cis-trans isomerization of peptidyl-prolyl bonds in polypeptide chains, thereby significantly accelerating protein folding. As a result, PPIases play critical roles in a wide range of physiological processes mediated by their substrate proteins. Myxobacteria are distinguished by their complex multicellular social behaviors. Among the 17 PPIases belonging to three families in Myxococcus xanthus DK1622, the membrane-bound Pin3, one of the SurA homologs, is involved in social behaviors such as social motility, predation, and sporulation. Given that PPIases are widely recognized as chaperones, our results also indicate that these M. xanthus PPIases extensively contribute to stress tolerance. Our findings underscore the essential functions of PPIases in cellular processes and reveal a correlation between the expansion of cellular functionalities and the functional evolution of PPIase proteins. Peptidylprolyl isomerase (PPIase), a ubiquitous enzyme present across nearly all kingdoms of life, catalyzes the cis-trans isomerization of peptidyl-prolyl bonds in polypeptide chains, thereby significantly accelerating protein folding. As a result, PPIases play critical roles in a wide range of physiological processes mediated by their substrate proteins. Myxobacteria are distinguished by their complex multicellular social behaviors. Among the 17 PPIases belonging to three families in Myxococcus xanthus DK1622, the membrane-bound Pin3, one of the SurA homologs, is involved in social behaviors such as social motility, predation, and sporulation. Given that PPIases are widely recognized as chaperones, our results also indicate that these M. xanthus PPIases extensively contribute to stress tolerance. Our findings underscore the essential functions of PPIases in cellular processes and reveal a correlation between the expansion of cellular functionalities and the functional evolution of PPIase proteins.
Tian-yu Wan, Rui-You Chen, Zi-Ye Zhou et al.· Applied and Environmental Mi...· 0 citations
