Abstract
Anaerobic ammonium-oxidizing (anammox) bacteria, members of the “Candidatus Brocadiaceae” family, play an important role in the nitrogen cycle and are estimated to be responsible for about half of the oceanic nitrogen loss to the atmosphere. Anammox bacteria combine ammonium with nitrite and produce dinitrogen gas via the intermediates nitric oxide and hydrazine (anammox reaction) while nitrate is formed as a by-product. These reactions take place in a specialized, membrane-enclosed compartment called the anammoxosome. Therefore, the substrates ammonium, nitrite and product nitrate have to cross the outer-, cytoplasmic-, and anammoxosome membranes to enter or exit the anammoxosome. The genomes of all anammox species harbor multiple copies of ammonium-, nitrite-, and nitrate transporter genes. Here we investigated how the distinct genes for ammonium-, nitrite-, and nitrate- transport were expressed during substrate limitation in membrane bioreactors. Transcriptome analysis of Kuenenia stuttgartiensis planktonic cells showed that four of the seven ammonium transporter homologs and two of the nine nitrite transporter homologs were significantly upregulated during ammonium-limited growth, while another ammonium transporter- and four nitrite transporter homologs were upregulated in nitrite limited growth conditions. The two nitrate transporters were expressed to similar levels in both conditions. In addition, genes encoding enzymes involved in the anammox reaction were differentially expressed, with those using nitrite as a substrate being upregulated under nitrite limited growth and those using ammonium as a substrate being upregulated during ammonium limitation. Taken together, these results give a first insight in the potential role of the multiple nutrient transporters in regulating transport of substrates and products in and out of the compartmentalized anammox cell.
Highlights
Anaerobic ammonium-oxidizing bacteria play a major role in the biological nitrogen cycle where they contribute significantly to oceanic nitrogen loss and are estimated to be responsible for up to 50% of the dinitrogen gas release to the atmosphere (Francis et al, 2007; Lam and Kuypers, 2011)
Anammox cells grow generally in larger cell aggregates, the “type strain” Kuenenia stuttgartiensis and Brocadia sinica can be cultivated as a planktonic enrichment culture
The expression of the multiple ammonium, nitrite and nitrate transporters encoded in the genome of K. stuttgartiensis MBR1 was studied under ammonium- and nitrite limited growth conditions
Summary
Anaerobic ammonium-oxidizing (anammox) bacteria play a major role in the biological nitrogen cycle where they contribute significantly to oceanic nitrogen loss and are estimated to be responsible for up to 50% of the dinitrogen gas release to the atmosphere (Francis et al, 2007; Lam and Kuypers, 2011). They are applied in wastewater treatment for costeffective and environment-friendly nitrogen removal (Kartal et al, 2010; Lackner et al, 2014). Anammox cells grow generally in larger cell aggregates, the “type strain” Kuenenia stuttgartiensis and Brocadia sinica can be cultivated as a planktonic enrichment culture (van der Star et al, 2008; Zhang and Okabe, 2017)
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