Effects of sea animal colonization on the coupling between dynamics and activity of soil ammonia-oxidizing bacteria and archaea in maritime Antarctica

Abstract

The colonization by a large number of sea animals, including penguins and seals, plays an important role in the nitrogen cycle of the tundra ecosystem in coastal Antarctica. However, little is known about the effects of sea animal colonization on ammonia-oxidizing archaea (AOA) and bacteria (AOB) communities involved in nitrogen transformations. In this study, we chose active seal colony tundra soils (SSs), penguin colony soils (PSs), adjacent penguin-lacking tundra soils (PLs), tundra marsh soils (MSs), and background tundra soils (BSs) to investigate the effects of sea animal colonization on the abundance, activity, and diversity of AOA and AOB in maritime Antarctica. Results indicated that AOB dominated over AOA in PS, SS, and PL, whereas AOB and AOA abundances were similar in MS and BS. Penguin or seal activities increased the abundance of soil AOB amoA genes but reduced the abundance of AOA amoA genes, leading to very large ratios (1.5×102 to 3.2×104) of AOB to AOA amoA copy numbers. Potential ammonia oxidation rates (PAORs) were significantly higher (P=0.02) in SS and PS than in PL, MS, and BS and were significantly positively correlated (P<0.001) with AOB amoA gene abundance. The predominance of AOB over AOA and their correlation with PAOR suggested that AOB play a more important role in the nitrification in animal colony soils. Sequence analysis for gene clones showed that AOA and AOB in tundra soils were from the Nitrososphaera and Nitrosospira lineages, respectively. Penguin or seal activities led to a predominance of AOA phylotypes related to Nitrososphaera cluster I and AOB phylotypes related to Nitrosospira clusters I and II but very low relative abundances in AOA phylotypes related to cluster II, and AOB phylotypes related to clusters III and IV. The differences in AOB and AOA community structures were closely related to soil biogeochemical processes under the disturbance of penguin or seal activities: soil C : N alteration and sufficient input of NH4+–N and phosphorus from animal excrements. The results significantly enhanced the understanding of ammonia-oxidizing microbial communities in the tundra environment of maritime Antarctica.