The Indo-Australian basin, a unique oligotrophic pelagic region influenced by distinct major currents from the Eastern Indian and Pacific Oceans, remains poorly understood in terms of microbial community composition, biogeochemical processes, and distribution-regulating mechanisms. We collected 57 water samples spanning the surface layer to depths exceeding 5,000 m (including the euphotic, dysphotic, and aphotic zones) across four stations to investigate the biogeochemical conditions and its inhabiting microbial community. A primary nitrite maximum (PNM) was observed at 50-100 m, whereas the dissolved oxygen (DO) minimum occurred at 750-1,000 m. 16S rRNA gene amplicon sequencing revealed the distinct community compositions across oxygen gradients, shifting from phototrophic to chemoheterotrophic groups. Temperature, nutrients, and DO were primary drivers shaping the microbial community composition. Biomarker taxa were identified in different layers: Prochlorococcus MIT9313 and Clade Ia in the euphotic zone,
Nitrosopumilaceae and the SAR324 clade in the dysphotic zone, and
Alteromonadales and
Oceanospirillales in the aphotic zone. Co-occurrence network analysis identified the SAR324 clade and
Nitratireductor as keystone taxa that maintain network complexity and stability.
Candidatus Nitrosopelagicus was enriched at the PNM, while
Nitrosopumilaceae and the SAR324 clade dominated hypoxic waters (750-1,000 m), potentially contributing to the formation of low-oxygen conditions. Surface-originated taxa were found to be transported from the surface to depths > 5,000 m. Microbial community assembly processes shifted from stochastic to deterministic as depth increased. Our findings reveal the complex mechanisms governing microbial community distribution in the oligotrophic water column and advance our understanding of the microbially mediated biogeochemical cycling in the open oceans.