The extracellular-matrix-retaining cyanobacterium Nostoc verrucosum accumulates trehalose, but is sensitive to desiccation

Abstract

The aquatic cyanobacterium Nostoc verrucosum forms macroscopic colonies, which consist of both cellular filaments and massive extracellular matrix material. In this study, the physiological features of N. verrucosum were investigated and compared with those of the anhydrobiotic cyanobacterium Nostoc commune. Nostoc verrucosum cells were sensitive to desiccation, but tolerant of freeze-thawing treatment in terms of both cell viability and photosynthetic O(2) evolution. Natural colonies of these cyanobacteria contained similar levels of chlorophyll a, carotenoids, the UV-absorbing pigments scytonemin and mycosporine-like amino acids, and uronic acid [a component of extracellular polysaccharides (EPS)]. EPS from both N. verrucosum and N. commune indicated low acidity and a high affinity for divalent cations, although their sugar compositions differed. The WspA protein, known to be a major component of the extracellular matrix of N. commune, was detected in N. verrucosum. Desiccation caused similarly high levels of trehalose accumulation in both cyanobacteria. Although previously considered relevant to anhydrobiosis in the terrestrial cyanobacterium N. commune, the data presented here suggest that extracellular matrix production and trehalose accumulation are not enough for standing extreme desiccation in N. verrucosum.

Characterization of extracellular matrix components from the desiccation-tolerant cyanobacterium <i>Nostoc commune</i>

“…No wspA gene has been found in the genome of Nostoc punctiforme ATCC 29133 (Meeks et al, 2001), which is almost genetically indistinguishable from N. commune (Arima et al, 2012). Notably, the WspA protein is found in the extracellular matrix of the aquatic cyanobacterium Nostoc verrucosum (Sakamoto et al, 2011). N. verrucosum forms massive colonies with an extracellular matrix, the macroscopic and microscopic appearances of which are similar to those of N. commune, although N. verrucosum colonies always occur in streams and are sensitive to desiccation (Sakamoto et al, 2011).…”

“…The SodF protein with superoxide dismutase activity is also abundant as an extracellular matrix protein (Shirkey et al, 2000;Wright et al, 2005). The heterogeneic forms of the WspA proteins are often found in naturally growing field-isolated colonies of N. commune (Helm and Potts, 2012;Sakamoto et al, 2011;Scherer and Potts, 1989;Wright et al, 2005), although the wspA gene is cloned as a single genomic copy in the laboratory-cultured N. commune strain known as DRH1 (Wright et al, 2005) and N. commune strain KU002 (Sakamoto et al, 2011). No wspA gene has been found in the genome of Nostoc punctiforme ATCC 29133 (Meeks et al, 2001), which is almost genetically indistinguishable from N. commune (Arima et al, 2012).…”

“…The WspA protein is known as the most abundant protein component in the extracellular matrix of N. commune and accounts for approximately 80% of the extracellular water-soluble proteins (Morsy et al, 2008;Sakamoto et al, 2011;Scherer and Potts, 1989;Wright et al, 2005). The SodF protein with superoxide dismutase activity is also abundant as an extracellular matrix protein (Shirkey et al, 2000;Wright et al, 2005).…”

“…In addition to the accumulation of compatible solutes such as trehalose in response to desiccation (Hershkovitz et al, 1991;Higo et al, 2006;Sakamoto et al, 2009;Yoshida and Sakamoto, 2009), EPS is thought to play a protective role against desiccation to maintain the structures and functions of biological membranes (Chakraborty and Pal, 2014). Given its expected role in desiccation tolerance, the N. commune EPS shows a high water-absorbing capacity and a moisture-retention property (Li et al, 2011;Sakamoto et al, 2011;Shaw et al, 2003;Tamaru et al, 2005). However, studies on the involvement of EPS in the molecular mechanism of desiccation tolerance are limited (Hill et al, 1994(Hill et al, , 1997.…”

“…We have studied the desiccation tolerance in N. commune in physiological and biochemical terms (Matsui et al, 2011(Matsui et al, , 2012Morsy et al, 2008;Nazifi et al, 2013Nazifi et al, , 2015Sakamoto et al, 2009Sakamoto et al, , 2011Tamaru et al, 2005;Yoshida and Sakamoto, 2009;Wada et al, 2013Wada et al, , 2015.…”