The secretion of ligninolytic enzyme provides a competitive advantage for microbial survival. These enzymes are commonly transported to the extracellular milieu via signal peptides for the catabolism of lignin, which cannot be translocated through the cell membrane. However, some bacterial ligninolytic enzymes lack signal peptides, yet they can still be secreted. It remains unclear how these unconventional proteins cross the cell membrane. Here, we reveal a secretion mechanism for the unconventional B-type dye-decolorizing peroxidase (DypB) in Pseudomonas putida A514. Type VI secretion system (T6SS) mediates the inner membrane channel, where interaction of DypB with the T6SS components VgrG and Hcp accounts for periplasmic delivery. Once in the periplasm, DypB is allocated into outer membrane vesicles (OMVs) and released to the extracellular space. The crosslinked translocation model for DypB delivery represents an ingenious mechanism by which bacteria harness extant systems to thrive in a nutrient-poor environment. Moreover, we develop an OMV-surface display platform to improve DypB secretion and further enhance lignin utilization, exemplifying the applicability of OMVs as a lignin biocatalytic nanoreactor. Our study demonstrates the previously unrecognized crosslinking of T6SS and OMVs for the secretion of unconventional ligninolytic peroxidase and provides new perspectives on its biotechnological applications.