Abstract
Marine Thaumarchaeota were discovered over 20 years ago and although a few isolates from this group are now available for study, we do not yet understand the environmental controls on their growth and distribution. Thaumarchaeotes oxidize ammonia to nitrite, mediating a key step in the global nitrogen cycle, and it is estimated that about 20% of all prokaryotic cells in the ocean belong to this phylum. Despite their almost ubiquitous distribution, marine Thaumarchaeota are rarely abundant in open-ocean surface (<100 m) waters. We tested the hypothesis that this vertical distribution is driven by reactive oxygen species (ROS), specifically H2O2, generated by photochemical and biological processes – ‘indirect photoinhibition’ rather than light inhibition as previously postulated for ammonia-oxidizing Archaea. Here we show that H2O2 can be surprisingly toxic to Thaumarchaeota from the Southern Ocean, with ammonia oxidation inhibited by additions of as little as 10 nM H2O2, while temperate Thaumarchaeota ecotypes were more tolerant. This sensitivity could explain the seasonal disappearance of Thaumarchaeota from polar surface waters and the increase in ammonia oxidation rates with depth commonly observed in marine environments. Our results highlight the need for further physiological studies of Thaumarchaeota, and indicate that ROS sensitivity could be used as a characteristic for dividing the group into meaningful ecotypes.
Highlights
We examined the sensitivity of ammonia oxidation (AO) to the reactive oxygen species (ROS) species H2O2 in ammonia-oxidizing organisms (AOO) assemblages dominated by Thaumarchaeota (Supplementary Tables 2, 3) from a wide range of marine environments, including the Southern Ocean near Palmer Station (Antarctica), the Gulf of Mexico, the Gulf of Alaska, and coastal waters at Marsh Landing, Georgia, USA (See Materials and Methods for details; Figure 2)
AO rates were below detection in the Southern Ocean following the addition of 6–80 nM H2O2 to samples above in situ concentrations (Figures 4A,B; Table 1, Supplementary Table 6), indicating that AOO in this region are extremely sensitive to H2O2
Culture-based experiments testing light inhibition have indicated that AO by both ammonia-oxidizing Bacteria (AOB) (Hooper and Terry, 1973; Horrigan and Springer, 1990; Hyman and Arp, 1992; Guerrero and Jones, 1996a) and AOA (Merbt et al, 2012; Qin et al, 2014) is decreased in the presence of increased light; yet none of these studies measured ROS generation during their incubations, which can occur at rates of 10–600 nM H2O2 h−1 under simulated light conditions (Kieber et al, 2003, 2014; Powers and Miller, 2015)
Summary
Photoinhibition has been hypothesized to reduce ammonia oxidation (AO), the first step of nitrification, in both ammonia-oxidizing Bacteria (AOB; Hooper and Terry, 1973; Olson, 1981; Ward, 1985; Horrigan and Springer, 1990) and Archaea (AOA; Murray et al, 1998, 1999a; Church et al, 2003; Qin et al, 2014). Thaumarchaeota do not typically achieve high abundances in the surface ocean (Karner et al, 2001; Mincer et al, 2007), with notable exceptions during winter at higher latitudes and in polar regions (Murray et al, 1998, 1999a; Church et al, 2003; Wuchter et al, 2006) Attempts to explain these patterns have focused primarily on competition with Bacteria or phytoplankton and on light inhibition (Murray et al, 1999a; Church et al, 2003; Wells and Deming, 2003; Merbt et al, 2012; Smith et al, 2014b). This could indicate that photoinhibition or a product of increased irradiance (such as reactive oxygen species, or ROS) affects Thaumarchaeota and, perhaps, nitrification in general, as AOB have been shown to be sensitive to light (Hooper and Terry, 1973; Olson, 1981; Ward, 1985; Horrigan and Springer, 1990)
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