Chemoautotrophic growth of ammonia-oxidizing Thaumarchaeota enriched from a pelagic redox gradient in the Baltic Sea

Abstract

Ammonia-oxidizing archaea (AOA) are an important component of the planktonic community in aquatic habitats, linking nitrogen and carbon cycles through nitrification and carbon fixation. Therefore, measurements of these processes in culture-based experiments can provide insights into their contributions to energy conservation and biomass production by specific AOA. In this study, by enriching AOA from a brackish, oxygen-depleted water-column in the Landsort Deep, central Baltic Sea, we were able to investigate ammonium oxidation, chemoautotrophy, and growth in seawater batch experiments. The highly enriched culture consisted of up to 97% archaea, with maximal archaeal numbers of 2.9 × 107 cells mL−1. Phylogenetic analysis of the 16S rRNA and ammonia monooxygenase subunit A (amoA) gene sequences revealed an affiliation with assemblages from low-salinity and freshwater habitats, with Candidatus Nitrosoarchaeum limnia as the closest relative. Growth correlated significantly with nitrite production, ammonium consumption, and CO2 fixation, which occurred at a ratio of 10 atoms N oxidized per 1 atom C fixed. According to the carbon balance, AOA biomass production can be entirely explained by chemoautotrophy. The cellular carbon content was estimated to be 9 fg C per cell. Single-cell-based 13C and 15N labeling experiments and analysis by nano-scale secondary ion mass spectrometry provided further evidence that cellular carbon was derived from bicarbonate and that ammonium was taken up by the cells. Our study therefore revealed that growth by an AOA belonging to the genus Nitrosoarchaeum can be sustained largely by chemoautotrophy.

Carbon isotopes of dissolved inorganic carbon reflect utilization of different carbon sources by microbial communities in two limestone aquifer assemblages

“…Facultative chemolithoautotrophic bacteria like ammonia-oxidizing Nitrospirae or the thiosulfate-reducing Sulfuritalea (Kojima and Fukui, 2011) and the sulfur-oxidizing Sulfuricurvum (Kodama and Watanabe, 2004) were detected in well H-52, as well as chemolithoauotrophic ammonia-oxidizing Thau-marcheota (Berg et al, 2014), which constitute 90 % of total archaeal reads.…”

Global-Scale Structure of the Eelgrass Microbiome

“…The colonization of above- and belowground plant tissues by microorganisms from surrounding environments initiates interactions that are essential for plant productivity (1, 2), fitness (3, 4), and disease resistance (5–7). The drivers of plant microbiome structure and composition and the ways in which plant hosts acquire microorganisms from surrounding microbial species pools therefore have consequences for ecosystem dynamics, biodiversity, and agricultural productivity (8–11). Recent studies have identified critical associations between host and environmental factors and patterns of microbial community structure on plant compartments such as leaves (e.g., see references 12 and 13) and roots (e.g., see references 6 and 14).…”

Physiological Ecology of Microorganisms in Subglacial Lake Whillans

“…If we make the same assumptions as in our oxygen model (water inflow rate = 0.007 km 3 y −1 ; upstream water is geochemically identical to the water in SLW with NH${}_4^{+}$ = 3.3 μmol L −1 ; Table S1), then inflow from upstream adds 2.3 × 10 4 mol NH${}_4^{+}$ y −1 , for a total annual ammonium supply of 2.4 × 10 4 mol NH${}_4^{+}$ y −1 . The SLW water column ammonium demand is estimated to be as high as 1.3 × 10 6 mol NH${}_4^{+}$ y −1 , assuming all chemoautotrophic C-fixation is due to nitrification (2.7 nmol C L −1 d −1 ; Christner et al, 2014) and that the stoichiometry associated with chemoautotrophic nitrification is 10 mol N per mol of C fixed; Berg et al, 2015). Subtracting the demand (1.3 × 10 6 mol NH${}_4^{+}$ y −1 ) from the supply (2.4 × 10 4 mol NH${}_4^{+}$ y −1 ) leaves an annual ammonium deficit of 1.3 × 10 6 mol NH${}_4^{+}$ y −1 .…”

“…There is evidence that rates of chemosynthesis are higher at the sediment water interface (Mikucki et al, 2015); however, here we assume that the rate of carbon fixation was constant with depth over the area of the lake. The O 2 demand was calculated assuming 0.1 moles of carbon fixed for every mole of ammonium oxidized (Berg et al, 2015) and a stoichiometry for complete nitrification of NH${}_4^{+}$ to NO${}_3^{-}$ of 2 mol of O 2 per mol of nitrogen oxidized.…”