Microscale dynamics promote segregated denitrification in diatom aggregates sinking slowly in bulk oxygenated seawater

Abstract

Sinking marine particles drive the biological pump that naturally sequesters carbon from the atmosphere. Despite their small size, the compartmentalized nature of particles promotes intense localized metabolic activity by their bacterial colonizers. Yet the mechanisms promoting the onset of denitrification, a metabolism that arises once oxygen is limiting, remain to be established. Here we show experimentally that slow sinking aggregates composed of marine diatoms—important primary producers for global carbon export—support active denitrification even among bulk oxygenated water typically thought to exclude anaerobic metabolisms. Denitrification occurs at anoxic microsites distributed throughout a particle and within microns of a particle’s boundary, and fluorescence-reporting bacteria show nitrite can be released into the water column due to segregated dissimilatory reduction of nitrate and nitrite. Examining intact and broken diatoms as organic sources, we show slowly leaking cells promote more bacterial growth, allow particles to have lower oxygen, and generally support greater denitrification.

Physical structure and interstitial flows govern microbial life in microenvironments

“…For instance, soil bacterial hotspots such as aggregates and the rhizosphere 3 are important sources of greenhouse gases 4 due to the localized development of anoxic niches 5 . In the oceans, similar anoxic microenvironments are observed in settling marine snow 6,7 that support anaerobic metabolisms 8 and can nearly double the niche size for marine denitrification on a global scale 9 . The occurrence of anoxic microenvironments due to diffusive limitations is not exclusive to natural environments.…”

Microscale advection governs microbial growth and oxygen consumption in macroporous aggregates

“…For instance, soil bacterial hotspots, such as aggregates and the rhizosphere ( 3 ), are important sources of greenhouse gases ( 4 ) due to the localized development of anoxic niches ( 5 ). In the oceans, similar anoxic microenvironments are observed in settling marine snow ( 6 , 7 ) that support anaerobic metabolisms ( 8 ) and can nearly double the niche size for marine denitrification on a global scale ( 9 ). The occurrence of anoxic microenvironments due to diffusive limitations is not exclusive to natural environments.…”

“…We subsequently utilized this channel to measure the exact angle orientation, width, and length of the channel. Finally, we segmented the colonies, and their spatial positions relative to the channel and particle edges were obtained using methods described elsewhere ( 7 , 13 ).…”

“…We added nanoprobes at a final concentration of 50 µg mL −1 to the molten agarose before gel-casting the agarose slab. We visualized the fluorescence of the oxygen-sensitive nanoprobes using a Cy5 filter cube (excitation: 590–650 nm and emission: 662–737 nm) in 1-h intervals for 24 h. For each disc, we related the fluorescent intensity to the oxygen saturation using a two-point calibration ( 7 , 13 ). Oxygen-rich conditions were obtained from the initial image (T0, before bacterial growth).…”

Apparent nitrous acid dissociation across environmentally relevant temperatures in freshwater and seawater

“…It further is an intermediate in assimilatory nitrate reduction by phytoplankton and other microbes. Nitrite has been well described across the ocean, accumulating at predictable depth horizons below the euphotic zone (the primary nitrite maximum, PNM) (Lomas and Lipschultz, 2006;Zakem et al, 2018;Ciccarese et al, 2023), at anoxic marine depths in the oxygen deficient zones (the secondary nitrite maximum, SNM) (Ulloa et al, 2012;Babbin et al, 2014Babbin et al, , 2017Babbin et al, , 2020, and sometimes in marine sediments at the interface between oxic and anoxic layers (Zhao et al, 2023). Furthermore, global lakes ranging from large temperate basins to confined polar meromictic lakes can exhibit nitrite accumulation globally both in the water column and in underlying sediments, often elevated under eutrophic and low oxygen conditions (Vincent et al, 1981;Lee et al, 2004;Powers et al, 2017).…”