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Characterization of a new internal promoter (P₃) for Rhizobium leguminosarum hydrogenase accessory genes hupGHIJ

¹ Departamento de Biotecnología, E. T. S. de Ingenieros Agrónomos, Universidad Politécnica de Madrid, 28040 Madrid, Spain
² Consejo Superior de Investigaciones Científicas (C.S.I.C.), 28040 Madrid, Spain

Correspondence
Tomás Ruiz-Argüeso
ruizargueso{at}bit.etsia.upm.es

Synthesis of the Rhizobium leguminosarum [NiFe] hydrogenase requires the participation of 16 accessory genes (hupCDEFGHIJKhypABFCDEX) besides the genes encoding the structural proteins (hupSL). Transcription of hupSL is controlled by a -24/-12-type promoter (P₁), located upstream of hupS and regulated by NifA. In this work, a second -24/-12-type promoter (P₃), located upstream of the hupG gene and transcribing hupGHIJ genes in R. leguminosarum pea (Pisum sativum L.) bacteroids, has been identified in the hup gene cluster. Promoter P₃ was also active in R. leguminosarum free-living cells, as evidenced by genetic complementation of hydrogenase mutants. Both NifA and NtrC activated P₃ expression in the heterologous host Klebsiella pneumoniae. Also, P₃ activity was highly stimulated by K. pneumoniae NifA in Escherichia coli. This NifA activation of P₃ expression only required the ⁵⁴-binding site, and it was independent of any cis-acting element upstream of the ⁵⁴ box, which suggests a direct interaction of free NifA with the RNA polymerase holoenzyme. P₃-dependent hupGHIJ expression in pea nodules started in interzone II/III, spanned through nitrogen-fixing zone III, and was coincident with the NifA-dependent nifH expression pattern. However, P₃ was dispensable for hupGHIJ transcription and hydrogenase activity in pea bacteroids due to transcription initiated at P₁. This fact and the lack of an activator recruitment system suggest that P₃ plays a secondary role in symbiotic hupGHIJ expression.

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