Cyanobacterial Secretion Systems: Understanding Fundamental Mechanisms Toward Technological Applications

Gonçalves, Cátia F.; Lima, Steeve; Tamagnini, Paula; Oliveira, Paulo

doi:10.1016/b978-0-12-814667-5.00018-0

Cited by 11 publications

(10 citation statements)

References 228 publications

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“…Nevertheless, except for one gene encoding a putative secreted protein that is likely a distant homolog of the Hop effector protein (Table 5), which is also found in other cyanobacteria with a presumed function of kinase (Zhang et al, 2016), the type III secretion system as well as its effectors appear to be completely absent in the assembled Brasilonema genomes. This is in agreement with observations for other cyanobacteria showing that they present the types I, II and IV secretion systems, but not the type III (Gonçalves et al, 2019). Since the transmission of this secretion system can occur either by vertical or horizontal transfer (Jackson et al, 2011), its absence in Brasilonema spp.…”

Section: Discussionsupporting

confidence: 92%

EvaluatingEucalyptusleaf colonization byBrasilonema octagenarum(Cyanobacteria, Scytonemataceae) usingin plantaexperiments and genomics

Alvarenga

Franco

Sivonen

et al. 2020

PeerJ

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Background Brasilonema is a cyanobacterial genus found on the surface of mineral substrates and plants such as bromeliads, orchids and eucalyptus. B. octagenarum stands out among cyanobacteria due to causing damage to the leaves of its host in an interaction not yet observed in other cyanobacteria. Previous studies revealed that B. octagenaum UFV-E1 is capable of leading eucalyptus leaves to suffer internal tissue damage and necrosis by unknown mechanisms. This work aimed to investigate the effects of B. octagenarum UFV-E1 inoculation on Eucalyptus urograndis and to uncover molecular mechanisms potentially involved in leaf damage by these cyanobacteria using a comparative genomics approach. Results Leaves from E. urograndis saplings were exposed for 30 days to B. octagenarum UFV-E1, which was followed by the characterization of its genome and its comparison with the genomes of four other Brasilonema strains isolated from phyllosphere and the surface of mineral substrates. While UFV-E1 inoculation caused an increase in root and stem dry mass of the host plants, the sites colonized by cyanobacteria on leaves presented a significant decrease in pigmentation, showing that the cyanobacterial mats have an effect on leaf cell structure. Genomic analyses revealed that all evaluated Brasilonema genomes harbored genes encoding molecules possibly involved in plant-pathogen interactions, such as hydrolases targeting plant cell walls and proteins similar to known virulence factors from plant pathogens. However, sequences related to the type III secretory system and effectors were not detected, suggesting that, even if any virulence factors could be expressed in contact with their hosts, they would not have the structural means to actively reach plant cytoplasm. Conclusions Leaf damage by this species is likely related to the blockage of access to sunlight by the efficient growth of cyanobacterial mats on the phyllosphere, which may hinder the photosynthetic machinery and prevent access to some essential molecules. These results reveal that the presence of cyanobacteria on leaf surfaces is not as universally beneficial as previously thought, since they may not merely provide the products of nitrogen fixation to their hosts in exchange for physical support, but in some cases also hinder regular leaf physiology leading to tissue damage.

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Section: Discussionsupporting

confidence: 92%

EvaluatingEucalyptusleaf colonization byBrasilonema octagenarum(Cyanobacteria, Scytonemataceae) usingin plantaexperiments and genomics

Alvarenga

Franco

Sivonen

et al. 2020

PeerJ

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“…Thus, product export represents an important survival strategy, playing crucial roles in a number of aspects of cyanobacterial physiology, like motility [ 24 ], adhesion [ 25 ], protection against desiccation [ 26 ], detoxification of extracellular reactive oxygen species [ 8 , 27 ], noxious compound efflux [ 9 , 20 , 21 , 28 ], etc. Throughout the years, several reports have focused on the identification and characterization of molecular machines mediating the translocation of products of metabolism, and others across the cyanobacterial inner and outer membranes (for reviews, see [ 29 , 30 ]). These systems, in which substrates are transported to the extracellular space via secretory portals located at the cell’s inner and outer membranes, are classified as “classical secretion systems”.…”

Section: Introductionmentioning

confidence: 99%

Extracellular Vesicles: An Overlooked Secretion System in Cyanobacteria

Lima

Matinha-Cardoso

Tamagnini

et al. 2020

Life

Self Cite

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In bacteria, the active transport of material from the interior to the exterior of the cell, or secretion, represents a very important mechanism of adaptation to the surrounding environment. The secretion of various types of biomolecules is mediated by a series of multiprotein complexes that cross the bacterial membrane(s), each complex dedicated to the secretion of specific substrates. In addition, biological material may also be released from the bacterial cell in the form of vesicles. Extracellular vesicles (EVs) are bilayered, nanoscale structures, derived from the bacterial cell envelope, which contain membrane components as well as soluble products. In cyanobacteria, the knowledge regarding EVs is lagging far behind compared to what is known about, for example, other Gram-negative bacteria. Here, we present a summary of the most important findings regarding EVs in Gram-negative bacteria, discussing aspects of their composition, formation processes and biological roles, and highlighting a number of technological applications tested. This lays the groundwork to raise awareness that the release of EVs by cyanobacteria likely represents an important, and yet highly disregarded, survival strategy. Furthermore, we hope to motivate future studies that can further elucidate the role of EVs in cyanobacterial cell biology and physiology.

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“…However, we can only speculate on the precise manner through which the protein is sorted in the periplasm and translocated across the outer membrane. Secretion in cyanobacteria is poorly characterized, however, two potential routes are known: a one-step, Sec or Tat independent, cytoplasm-to-medium route and a two-step periplasmic route that relies on Sec or Tat to mediate translocation across the plasma membrane and requires the engagement of additional components for translocation across the outer membrane [23]. Genome-wide bioinformatics analysis have identified both secretion systems in S. elongatus PCC 7942: the one-step type I secretion system (T1SS) and the two-step type IV pilus (T4P) assembly system [61].…”

Section: Discussionmentioning

confidence: 99%

“…Therefore, throughout this article, we will refer to translocation of a protein across the plasma membrane, to the periplasm, as “export” and the active transport of a protein from the interior to the exterior of the cell as “secretion” [22]. Although protein export and secretion pathways in cyanobacteria have been studied for almost two decades, they remain poorly understood (see recent reviews [21, 23]). Proof-of-concept studies have shown that heterologous protein secretion in cyanobacteria is possible, however, these studies have generally utilized native signal peptides fused to reporter proteins and have suffered from low yields [24, 25].…”

Section: Introductionmentioning

confidence: 99%

Expression and secretion of a lytic polysaccharide monooxygenase by a fast-growing cyanobacterium

Russo

Zedler

Wittmann

et al. 2019

Biotechnol Biofuels

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Background Cyanobacteria have the potential to become next-generation cell factories due to their ability to use CO 2 , light and inorganic nutrients to produce a range of biomolecules of commercial interest. Synechococcus elongatus UTEX 2973, in particular, is a fast-growing, genetically tractable, cyanobacterium that has garnered attention as a potential biotechnological chassis. To establish this unique strain as a host for heterologous protein production, we aimed to demonstrate expression and secretion of the industrially relevant Tf AA10A, a lytic polysaccharide monooxygenase from the Gram-positive bacterium Thermobifida fusca. Results Two variations of Tf AA10A were successfully expressed in S. elongatus UTEX 2973: One containing the native N-terminal, Sec-targeted, signal peptide and a second with a Tat-targeted signal peptide from the Escherichia coli trimethylamine- N -oxide reductase (TorA). Although the TorA signal peptide correctly targeted the protein to the plasma membrane, the majority of the TorA- Tf AA10A was found unprocessed in the plasma membrane with a small fraction of the mature protein ultimately translocated to the periplasm. The native Sec signal peptide allowed for efficient secretion of Tf AA10A into the medium with virtually no protein being found in the cytosol, plasma membrane or periplasm. Tf AA10A was demonstrated to be correctly cleaved and active on the model substrate phosphoric acid swollen cellulose. Additionally, expression and secretion only had a minor impact on cell growth. The secretion yield was estimated at 779 ± 40 µg L −1 based on densitometric analysis. To our knowledge, this is the highest secretion yield ever registered in cyanobacteria. Conclusions We have shown for the first time high-titer expression and secretion of an industrially relevant and catalytically active enzyme in S. elongatus UTEX 2973. This proof-of-concept study will be valuable for the development of novel and sustainable applications in the fields of bioremediation and biocatalysis. Electronic supplementary material The online version of this article (10.1186/s13068-019-1416-9) contains supplementary material, which is available to authorized users.

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Cyanobacterial Secretion Systems: Understanding Fundamental Mechanisms Toward Technological Applications

Cited by 11 publications

References 228 publications

EvaluatingEucalyptusleaf colonization byBrasilonema octagenarum(Cyanobacteria, Scytonemataceae) usingin plantaexperiments and genomics

EvaluatingEucalyptusleaf colonization byBrasilonema octagenarum(Cyanobacteria, Scytonemataceae) usingin plantaexperiments and genomics

Extracellular Vesicles: An Overlooked Secretion System in Cyanobacteria

Expression and secretion of a lytic polysaccharide monooxygenase by a fast-growing cyanobacterium

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