UV Irradiation and Desiccation Modulate the Three-dimensional Extracellular Matrix of Nostoc commune (Cyanobacteria)

Deborah J Wright,Sue C Smith,Vinita Joardar,Siegfried Scherer,Jody Jervis,Andrew Warren,Richard F Helm,Malcolm Potts

doi:10.1074/jbc.m505961200

Deborah J Wright, Sue C Smith + Show 6 more

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https://doi.org/10.1074/jbc.m505961200

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Abstract

Cyanobacterium Nostoc commune can tolerate the simultaneous stresses of desiccation, UV irradiation, and oxidation. Acidic WspA, of approximately 33.6 kDa, is secreted to the three-dimensional extracellular matrix and accounts for greater than 70% of the total soluble protein. The wspA gene of N. commune strain DRH1 was cloned and found in a single genomic copy, in a monocistronic operon. Transcription of wspA and sodF (superoxide dismutase), and synthesis and secretion of WspA, were induced upon desiccation or UV-A/B irradiation of cells. Recombinant WspA binds the UV-A/B absorbing pigment scytonemin through non-covalent interactions. WspA peptide polymorphism, and heterogeneity of multiple wspA sequences within cells of a single colony, account for distinct WspA isoforms. WspA has no similarity to entries in the sequence databases and wspA, a possible xenolog, is restricted to a subset of strains in the "form species" N. commune characterized through group I intron phylogeny. We hypothesize that WspA plays a central role in the global stress response of N. commune through modulation of the structure and function of the three-dimensional extracellular matrix, particularly the transport, distribution, and/or macromolecular architecture of mycosporine and scytonemin UV-A/B absorbing pigment complexes.

Highlights

IntroductionThe principal components of this matrix are a diverse collection of secreted macromolecules including water stress protein (WspA)4 [9, 10], a highly stable and active superoxide dismutase (SodF) [11], water-soluble (mycosporine amino acids) [12] and lipid-soluble (scytonemin) [8, 13] UV absorbing pigments
When exposed to UV-A/B irradiation cultures of N. commune DRH1 increase the synthesis of WspA, extracellular glycan, mycosporine amino acids, scytonemin, and carotenoids [12]
UV-A/B irradiation and desiccation induced the expression of wspA and sodF, which lead to elevated synthesis and secretion of WspA and SodF

Summary

Introduction

The principal components of this matrix are a diverse collection of secreted macromolecules including water stress protein (WspA)4 [9, 10], a highly stable and active superoxide dismutase (SodF) [11], water-soluble (mycosporine amino acids) [12] and lipid-soluble (scytonemin) [8, 13] UV absorbing pigments. All of these components are distributed within a secreted high molecular weight extracellular polysaccharide, a glycan [14], which has unusual rheological properties and constitutes the bulk of desiccated and rehydrated colonies [14, 15]. Cyanobacteria reference numbers of form species include a mnemonic of the place of origin and the year the sample was desiccated (see Table I in Ref. 3; see text Fig. 2D)

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