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The high availability of electron donors occurring in coastal upwelling ecosystems with marked oxyclines favours chemoautotrophy, in turn leading to high N₂O and CH₄ cycling associated with aerobic NH₄⁺ (AAO) and CH₄ oxidation (AMO). This is the case of the highly productive coastal upwelling area off central Chile (36° S), where we evaluated the importance of total chemolithoautotrophic vs. photoautotrophic production, the specific contributions of AAO and AMO to chemosynthesis and their role in gas cycling. Chemolithoautotrophy was studied at a time-series station during monthly (2007–2009) and seasonal cruises (January 2008, September 2008, January 2009) and was assessed in terms of the natural C isotopic ratio of particulate organic carbon (δ¹³POC), total and specific (associated with AAO and AMO) dark carbon assimilation (CA), and N₂O and CH₄ cycling experiments. At the oxycline, δ¹³POC averaged −22.2‰; this was significantly lighter compared to the surface (−19.7‰) and bottom layers (−20.7‰). Total integrated dark CA in the whole water column fluctuated between 19.4 and 2.924 mg C m^−2 d^−1, was higher during active upwelling, and contributed 0.7 to 49.7% of the total integrated autotrophic CA (photo plus chemoautotrophy), which ranged from 135 to 7.626 mg C m^−2 d^−1, and averaged 20.3% for the whole sampling period. Dark CA was reduced by 27 to 48% after adding a specific AAO inhibitor (ATU) and by 24 to 76% with GC7, a specific archaea inhibitor. This indicates that AAO and AMO microbes (most of them archaea) were performing dark CA through the oxidation of NH₄⁺ and CH₄. Net N₂O cycling rates varied between 8.88 and 43 nM d^−1, whereas net CH₄ cycling rates ranged from −0.41 to −26.8 nM d^−1. The addition of both ATU and GC7 reduced N₂O accumulation and increased CH₄ consumption, suggesting that AAO and AMO were responsible, in part, for the cycling of these gases. These findings show that chemically driven chemolithoautotrophy (with NH₄⁺ and CH₄ acting as electron donors) could be more important than previously thought in upwelling ecosystems, raising new questions concerning its relevance in the future ocean.