Melioidosis, caused by the bacterium Burkholderia pseudomallei, is an often-severe infection that regularly involves respiratory disease following inhalation exposure. Intra-nasal (i.n.) inoculation in mice represents an experimental approach to study the contributions of bacterial capsular polysaccharide I (CPS I) to virulence during acute disease. We used aerosol delivery of B. pseudomallei to establish respiratory infection in mice and studied CPS I in the context of innate immune responses. CPS I improved B. pseudomallei survival in vivo, and triggered multiple cytokine responses, neutrophil infiltration and acute inflammatory histopathology in Spleen, Liver, nasal-associated lymphoid tissue (NALT) and olfactory mucosa (OM). To further explore the role of the OM response to B. pseudomallei infection we infected human olfactory ensheathing cells (OECs) in vitro and measured bacterial invasion and the cytokine responses induced following infection. Human OECs killed >90% of B. pseudomallei in a CPS I independent manner and exhibited an antibacterial cytokine response comprising G-CSF, TNF-alpha and several regulatory cytokines. In-depth genome-wide transcriptomic profiling of the OEC response using RNA sequencing revealed a network of signalling pathways activated in OECs following infection; involving a novel group of 378 genes that encode biological pathways controlling cellular movement, inflammation, immunological disease and molecular transport. This represents the first antimicrobial program to be described in human OECs and establishes the extensive transcriptional defence network accessible within these cells. Collectively, these findings show a role of CPS I in B. pseudomallei survival in vivo following inhalation infection, and the antibacterial signalling network that exists in human OM and OECs.