Temperature response of denitrification and anammox reveals the adaptation of microbial communities to in situ temperatures in permeable marine sediments that span 50° in latitude

Abstract

Abstract. Despite decades of research on the physiology and biochemistry of nitrate/nitrite-respiring microorganisms, little is known regarding their metabolic response to temperature, especially under in situ conditions. The temperature regulation of microbial communities that mediate anammox and denitrification was investigated in near shore permeable sediments at polar, temperate, and subtropical sites with annual mean temperatures ranging from −5 to 23 °C. Total N2 production rates were determined using the isotope pairing technique in intact core incubations under diffusive and simulated advection conditions and ranged from 2 to 359 μmol N m−2 d−1. For the majority of sites studied, N2 removal was 2–7 times more rapid under simulated advective flow conditions. Anammox comprised 6–14% of total N2 production at temperate and polar sites and was not detected at the subtropical site. Potential rates of denitrification and anammox were determined in anaerobic slurries in a temperature gradient block incubator across a temperature range of −1 °C to 42 °C. The highest optimum temperature (Topt) for denitrification was 36 °C and was observed in subtropical sediments, while the lowest Topt of 21 °C was observed at the polar site. Seasonal variation in the Topt was observed at the temperate site with values of 26 and 34 °C in winter and summer, respectively. The Topt values for anammox were 9 and 26 °C at the polar and temperate sites, respectively. The results demonstrate adaptation of denitrifying communities to in situ temperatures in permeable marine sediments across a wide range of temperatures, whereas marine anammox bacteria may be predominately psychrophilic to psychrotolerant. The adaptation of microbial communities to in situ temperatures suggests that the relationship between temperature and rates of N removal is highly dependent on community structure.

Nitrogen Losses in Sediments of the East China Sea: Spatiotemporal Variations, Controlling Factors, and Environmental Implications

“…The high temperature during summer (21.9 ± 2.0°C) likely enhances sediment oxygen consumption and thus provides favorable anoxic conditions (Gardner & McCarthy, ; Wenk et al, ). These results agree with measurements of laboratory incubations to examine temperature responses of N‐loss rates in sediments (Brin, Giblin, & Rich, ; Canion et al, ; Canion et al, ; Dosta et al, ; Kawagoshi et al, ). However, the N‐loss rates measured under in situ‐like conditions varied little with season and did not correlate with temperature, especially for anammox (Heiss, Fields, & L. , & Fulweiler, R. W., ).…”

Temperature response of denitrification and anaerobic ammonium oxidation rates and microbial community structure in Arctic fjord sediments

“…This interpretation is further supported by optimal growth temperatures for denitrifying isolates from the same sites at Svalbard, which were shown to be within a range (5–15°C) consistent with the traditional definition of psychrophiles (Canion et al ., ). Additionally, a distinct T opt at 35°C has been previously observed in sediments where the predominant temperature adaptation of denitrification was mesophilic (King and Nedwell, ; Canion et al ., ).…”

Metabolic specialization of denitrifiers in permeable sediments controls N2O emissions

“…In fact, denitrification rates have been shown to be generally high in permeable sandy sediments even in subtidal regions (Canion et al . , Evrard et al ., , Gihring et al ., , Rao et al, , Sokoll et al, ) and there is evidence to suggest that N 2 O production rates are also high in subtidal sands (Marchant et al, ). The consistency of these studies support a recent estimate that 60% of fixed N input from rivers and atmospheric deposition worldwide is denitrified within coastal sandy sediments (equating to 54 Tg) (Gao et al ., ).…”