Growth of soil ammonia-oxidizing archaea on air-exposed solid surface

Abstract

Soil microorganisms often thrive as microcolonies or biofilms within pores of soil aggregates exposed to the soil atmosphere. However, previous studies on the physiology of soil ammonia-oxidizing microorganisms (AOM), which play a critical role in the nitrogen cycle, were primarily conducted using freely suspended AOM cells (planktonic cells) in liquid media. In this study, we examined the growth of two representative soil ammonia-oxidizing archaea (AOA),Nitrososphaera viennensisEN76 and “Nitrosotenuis chungbukensis” MY2, and an ammonia-oxidizing bacterium,Nitrosomonas europaeaATCC 19718 on polycarbonate membrane filters floated on liquid media to observe their adaptation to air-exposed solid surfaces. Interestingly, ammonia oxidation activities ofN. viennensisEN76 and “N. chungbukensis” MY2 were significantly repressed on floating filters compared to the freely suspended cells in liquid media. Conversely, the ammonia oxidation activity ofN. europaeaATCC 19718 was comparable on floating filters and liquid media.N. viennensisEN76 andN. europaeaATCC 19718 developed microcolonies on floating filters. Transcriptome analysis ofN. viennensisEN76 floating filter-grown cells revealed upregulation of unique sets of genes for cell wall and extracellular polymeric substance biosynthesis, H2O2-induced oxidative stress defense, and ammonia oxidation, including ammonia monooxygenase subunit C (amoC3) and the multicopper oxidases. These genes may play a pivotal role in adapting AOA to air-exposed solid surfaces. Furthermore, the floating filter technique resulted in the enrichment of distinct soil AOA communities dominated by the “Ca. Nitrosocosmicus” clade. Overall, this study sheds light on distinct adaptive mechanisms governing AOA growth on air-exposed solid surfaces.