Physical, Chemical and Proteomic Evidence of Potato Suberin Degradation by the Plant Pathogenic Bacterium <i>Streptomyces scabiei</i>

Abstract

Potato peels consist of a tissue called phellem, which is formed by suberized cell layers. The degradation of suberin, a lipidic and recalcitrant polymer, is an ecological process attributed to soil fungal populations; however, previous studies have suggested that Streptomyces scabiei, the causal agent of potato common scab, possesses the ability to degrade suberin. In the present study, S. scabiei was grown in medium containing suberin-enriched potato phellem as the sole carbon source and its secretome was analyzed periodically (10- to 60-d-old cultures) with a special focus on proteins potentially involved in cell wall degradation. Although the amount and diversity of proteins linked to polysaccharide degradation remained high throughout the experiment, their abundance decreased over time. In contrast, proteins dedicated to lipid metabolism represented a small fraction of the secretome; however, their abundance increased during the experiment. The lipolytic enzymes detected may be involved in the degradation of the aliphatic fraction of suberin because the results of optical and transmission electron microscopy examinations revealed a loss in the integrity of suberized tissues exposed to S. scabiei cells. Chemical analyses identified a time period in which the concentration of aliphatic compounds in potato phellem decreased and the sugar concentration increased; at the end of the 60-d incubation period, the sugar concentration in potato phellem was significantly reduced. This study demonstrated the ability of S. scabiei to degrade the aliphatic portion of suberin.

Enzymatic Degradation of <i>p</i>-Nitrophenyl Esters, Polyethylene Terephthalate, Cutin, and Suberin by Sub1, a Suberinase Encoded by the Plant Pathogen <i>Streptomyces scabies</i>

“…Although suberin degradation has not yet been examined in detail, some fungal cutinases exhibit activity towards suberin (Kontkanen et al, 2009). The protein Sub1 is part of the S. scabies secretome when this bacterium is grown in the presence of suberin (Beaulieu et al, 2016) and the sub1 gene is induced in the presence of suberin (Komeil et al, 2013). This study predicted that Sub1 was a cutinase due to its high sequence homology with other cutinases of fungal origin.…”

“…The extracted material was dried under a hood, ground using a coffee mill, and stored at room temperature. To further remove residual polysaccharides in the potato periderm, this material was exposed to microbial degradation in the presence of S. scabies EF-35, as described by Beaulieu et al (2016). The S. scabies inoculum (1 mL) was added to 50 mL of minimal medium consisting of a mineral solution (0.5 g L -1 [NH 4 ] 2 SO 4 , 0.5 g L -1 K 2 HPO 4 , 0.2 g L -1 MgSO 4 -7H 2 O, and 10 mg L -1 FeSO 4 -7H 2 O) and 1 g L -1 of the suberin-enriched potato periderm.…”

“…Common scab is characterized by corky lesions on the surface of potato tubers. Similar to other soil-inhabiting streptomycetes, S. scabies produces a large variety of extracellular enzymes, including various glycosyl hydrolases and esterases (Komeil et al, 2013;Beaulieu et al, 2016). These enzymes may participate in pathogenesis because the penetration of S. scabies into host plants is considered to be facilitated by the secretion of extracellular cell wall-degrading enzymes (Beauséjour et al, 1999).…”

“…This pathogenic bacterium exhibits strong esterase activity in the presence of suberized tissues (Beauséjour et al, 1999). Furthermore, a secretome analysis of S. scabies cultures grown in the presence of suberin revealed the presence of esterases, which are predicted to play a role in lipid metabolism (Komeil et al, 2014;Beaulieu et al, 2016). Among them, the Sub1 protein exhibits 33% identity with the cutinase CcCUT1 of the fungus C. cinerea (Komeil et al, 2013).…”

Chitinolytic functions in actinobacteria: ecology, enzymes, and evolution

“…scabies , when grown in the presence of potato periderm, produces over 200 different extracellular proteins which mostly are glycosyl hydrolases (Beaulieu et al 2016 ). In nature, actinobacterial extracellular enzymes are involved, among others, in the degradation of complex or recalcitrant biopolymers such as lignocellulose (Book et al 2014 ; Goodfellow 1983 ; Padilla-Reynaud et al 2015 ; Wang et al 2016 ), keratin (Mukhtar et al 2017 ), suberin (Beaulieu et al 2016 ) and chitin (Beier and Bertilsson 2013 ). This review is focused on the degradation of chitin and chitosan with emphasis on natural environments, molecular families of the genes, and proteins involved in these processes and their evolutionary relationships.…”