Traffic of Secondary Metabolites to Cell Surface in the Red Alga Laurencia dendroidea Depends on a Two-Step Transport by the Cytoskeleton

Reis, Vanessa M.; Oliveira, Louisi Souza de; Passos, Raoni Moreira Ferreira; Viana, Nathan B.; Mermelstein, Cláudia; Sant’Anna, Celso; Pereira, Renato Crespo; Paradas, Wladimir Costa; Thompson, Fabiano L.; Amado‐Filho, Gilberto M.; Salgado, Leonardo T.

doi:10.1371/journal.pone.0063929

Cited by 21 publications

(21 citation statements)

References 57 publications

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“…For chemical defense at the surface level, these metabolites are intracellularly mobilized through vesicle transport from the "corps en cerise" to the cell periphery for their posterior exocytosis. The cell structures involved in this specific vesicle traffic, as well as the cellular structures related to the positioning and anchoring of the "corps en cerise" within the cell are not well known [63].…”

Section: "Corps En Cerise"mentioning

confidence: 99%

The Laurencia Paradox: An Endless Source of Chemodiversity

Harizani

Iοannou

Roussis

2016

Progress in the Chemistry of Organic Natural Products

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Nature, the most prolific source of biological and chemical diversity, has provided mankind with treatments for health problems since ancient times and continues to be the most promising reservoir of bioactive chemicals for the development of modern drugs. In addition to the terrestrial organisms that still remain a promising source of new bioactive metabolites, the marine environment, covering approximately 70% of the Earth's surface and containing a largely unexplored biodiversity, offers an enormous resource for the discovery of novel compounds. According to the MarinLit database, more than 27,000 metabolites from marine macro- and microorganisms have been isolated to date providing material and key structures for the development of new products in the pharmaceutical, food, cosmeceutical, chemical, and agrochemical sectors. Algae, which thrive in the euphotic zone, were among the first marine organisms that were investigated as sources of food, nutritional supplements, soil fertilizers, and bioactive metabolites.Red algae of the genus Laurencia are accepted unanimously as one of the richest sources of new secondary metabolites. Their cosmopolitan distribution, along with the chemical variation influenced to a significant degree by environmental and genetic factors, have resulted in an endless parade of metabolites, often featuring multiple halogenation sites.The present contribution, covering the literature until August 2015, offers a comprehensive view of the chemical wealth and the taxonomic problems currently impeding chemical and biological investigations of the genus Laurencia. Since mollusks feeding on Laurencia are, in many cases, bioaccumulating, and utilize algal metabolites as chemical weaponry against natural enemies, metabolites of postulated dietary origin of sea hares that feed on Laurencia species are also included in the present review. Altogether, 1047 secondary metabolites, often featuring new carbocyclic skeletons, have been included.The chapter addresses: (1) the "Laurencia complex", the botanical description and the growth and population dynamics of the genus, as well as its chemical diversity and ecological relations; (2) the secondary metabolites, which are organized according to their chemical structures and are classified into sesquiterpenes, diterpenes, triterpenes, acetogenins, indoles, aromatic compounds, steroids, and miscellaneous compounds, as well as their sources of isolation which are depicted in tabulated form, and (3) the biological activity organized according to the biological target and the ecological functions of Laurencia metabolites.

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Section: "Corps En Cerise"mentioning

confidence: 99%

The Laurencia Paradox: An Endless Source of Chemodiversity

Harizani

Iοannou

Roussis

2016

Progress in the Chemistry of Organic Natural Products

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“…, Reis et al. ). The metabolites are then exocytosed at the CW and reach the algal surface, where they act as AF chemicals (Salgado et al.…”

mentioning

confidence: 99%

“…With regard to the exudation mechanisms of secondary metabolites, in brown algae, for example, 226 the Golgi apparatus plays a role in the synthesis and transport of phlorotannins to the cell wall (CW) via the exocytic pathway (Schoenwaelder 2002). In Laurencia dendroidea (Rhodophyta), exudation occurs by way of a complex system involving the microfilament-and microtubule-mediated vesicular transport of halogenated metabolites from corps en cerise (storage sites) to the cell periphery , Paradas et al 2010, Reis et al 2013. The metabolites are then exocytosed at the CW and reach the algal surface, where they act as AF chemicals , Paradas et al 2010.…”

mentioning

confidence: 99%

Mevalonosomes: specific vacuoles containing the mevalonate pathway in Plocamium brasiliense cortical cells (Rhodophyta)

Paradas

Crespo

Salgado

et al. 2015

Journal of Phycology

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This paper has identified, for the first time in a member of the Rhodophyta, a vacuolar organelle containing enzymes that are involved in the mevalonate pathway-an important step in red algal isoprenoid biosynthesis. These organelles were named mevalonosomes (Mev) and were found in the cortical cells (CC) of Plocamium brasiliense, a marine macroalgae that synthesizes several halogenated monoterpenes. P. brasiliense specimens were submitted to a cytochemical analysis of the activity of the 3-hydroxy-3-methylglutaryl-CoA synthase (HMGS). Using transmission electron microscopy (TEM), we confirmed the presence of HMGS activity within the Mev. Because HMGS is necessary for the biosynthesis of halogenated monoterpenes, we isolated a hexanic fraction (HF) rich in halogenated monoterpenes from P. brasiliense that contained a pentachlorinated monoterpene as a major metabolite. Because terpenes are often related to chemical defense, the antifouling (AF) activity of pentachlorinated monoterpene was tested. We found that the settlement of the mussel Perna perna was reduced by HF treatment (2.25 times less than control; 40% and 90% of fouled surface, respectively; P = 0.001; F9,9 = 1.13). The HF (at 10 μg · mL(-1) ) also inhibited three species of fouling microalgae (Chlorarachnion reptans, Cylindrotheca cloisterium, and Exanthemachrysis gayraliae), while at a higher concentration (50 μg · mL(-1) ), it inhibited the bacteria Halomonas marina, Polaribacter irgensii, Pseudoalteromonas elyakovii, Shewanella putrefaciens, and Vibrio aestuarianus. The AF activity of P. brasiliense halogenated monoterpenes and the localization of HMGS activity inside Mev suggest that this cellular structure found in CC may play a role in thallus protection against biofouling.

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“…Also vesicles containing other secondary metabolites with defensive attributes may be transported via the cytoskeleton (e.g., Reis et al. ). Therefore, reorganization of the cytoskeleton throughout the induction phase may be related to the healing of wounds caused by continuous exposure to grazing and/or transport of defense metabolites.…”

Section: Discussionmentioning

confidence: 99%

Induced resistance to periwinkle grazing in the brown seaweed Fucus vesiculosus (Phaeophyceae): molecular insights and seaweed‐mediated effects on herbivore interactions

Flöthe

Molis

John

2014

Journal of Phycology

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Herbivory is a key factor for controlling seaweed biomass and community structure. To cope with grazers, constitutive and inducible defenses have evolved in macroalgae. Inducible chemical defenses show grazer-specificity and, at the same time, have the potential to mediate interactions among different herbivores. Furthermore, temporal variations in defense patterns, which may adjust antiherbivory responses to grazing pressure, were reported in two brown seaweeds. However, underlying cellular processes are only rudimentarily characterized. To investigate the response of Fucus vesiculosus (L.) to periwinkle (Littorina obtusata) grazing, feeding assays were conducted at several times during a 33 d induction experiment. Underlying cellular processes were analyzed through gene expression profiling. Furthermore, direct processes driving the antiherbivory response to periwinkle grazing and indirect effects on another herbivore, the isopod Idotea baltica, were elucidated. F. vesiculosus showed multiple defense pulses in response to periwinkle grazing, suggesting a high level of temporal variability in antiherbivory traits. Defense induction was accompanied by extensive transcriptome changes. Approximately 400 genes were significantly up-/down-regulated relative to controls, including genes relevant for translation and the cytoskeleton. Genes involved in photosynthesis were mostly downregulated, while genes related to the respiratory chain were up-regulated, indicating alterations in resource allocation. The comparison of genes regulated in response to isopod (previous study) and periwinkle grazing suggests specific induction of several genes by each herbivore. However, grazing by both herbivores induced similar metabolic processes in F. vesiculosus. These common defense-related processes reflected in strong indirect effects as isopods were also repelled after previous grazing by L. obtusata.

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Traffic of Secondary Metabolites to Cell Surface in the Red Alga Laurencia dendroidea Depends on a Two-Step Transport by the Cytoskeleton

Cited by 21 publications

References 57 publications

The Laurencia Paradox: An Endless Source of Chemodiversity

The Laurencia Paradox: An Endless Source of Chemodiversity

Mevalonosomes: specific vacuoles containing the mevalonate pathway in Plocamium brasiliense cortical cells (Rhodophyta)

Induced resistance to periwinkle grazing in the brown seaweed Fucus vesiculosus (Phaeophyceae): molecular insights and seaweed‐mediated effects on herbivore interactions

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