Untargeted metabolomics used to describe the chemical composition and antimicrobial effects of the essential oil from the leaves of Guatteria citriodora Ducke
Graphical Abstract
Introduction
The Amazon region has great prominence due to it housing the largest area of rainforest in the world. In this ecosystem, about 11% of the world’s tree species are found (Cardoso et al., 2017), and it is estimated that there are around 50 000 vascular plant species (Hubbell et al., 2008). A recent study on the number of trees on Earth indicates the existence of ∼73 000 tree species (Gatti et al., 2022), while the survey of the number of trees in the Amazon region suggests ∼16 000 Amazonian tree species (Ter Steege et al., 2016). Given this scenario, the rational and sustainable use of tropical forest products (e.g., leaves, nuts, seeds, bark, resins, and oils) can potentially contribute to the preservation of forests and resources, in addition to promoting a source of income for the native population, which is especially important for poor rural communities (Nascimento et al., 2019; Mello et al., 2020). Therefore, studies have been conducted to evaluate the active ingredients found in Amazon biodiversity, as well as their use in pharmacology, cosmetics, and agriculture. Among the forest products, essential oils (EOs) have aroused great scientific interest since they encompass volatile molecules, which have aromatic features of biotechnological and industrial interest (Ricardo et al., 2017, da Silva et al., 2018, Souza et al., 2020).
EOs are characterized as complex mixtures of volatile substances, which are generally lipophilic and water-insoluble, and are mainly produced in flowers and leaves, but are also present in stems and bark, though to a lesser extent in seeds and roots ( Morone-Fortunato et al., 2010; Calvo-Irabien, 2018). Molecules of EOs are biosynthesized, accumulated and secreted in specialized anatomical structures such as secretory idioblasts, canals, cavities/ducts, or glandular trichomes (Pickard, 2008, Tiwari, 2016). The majority of compounds normally found in Eos, mainly originate from three biosynthetic pathways, (1) the plastidal 2-C-methylerythritol-4-phosphate (MEP) pathway, which leads to mono- and diterpenes, (2) the mevalonic acid (MVA) pathway, which acts in the cytosol producing sesquiterpenes, and (3) the shikimate pathway that leads to benzenoid derivatives (Bergman and Phillips, 2020, Rehman et al., 2016).
The biological properties of EOs have been known for a long time. Previous reports have shown the biotechnological potential of EOs, which is due their wide-spectrum of biological activities, and the fact that they are eco-friendly (Issa et al., 2020, Xiang et al., 2020, Yilmaz, 2020). Several biological activities of EOs, such as insecticidal, antiparasitic, antiviral, antibacterial and antifungal activity (Battisti et al., 2021, Sobrinho et al., 2021, Vega Gomez et al., 2021), have been shown in the literature. In vitro studies have shown that essential oils are active against bacteria and fungi and act mainly by disrupting cell membrane integrity by inducing an increase in the permeability of the membrane and the leakage of genetic material (Al-Shuneigat et al., 2020, Silva et al., 2019, Xu et al., 2018, Zhang et al., 2020).
Various EOs from plants that are endemic to the Amazon, including species of Burseraceae, Lauraceae, Cyperaceae, Piperaceae and Annonaceae (Maia and Andrade, 2009) have already been studied. Guatteria citriodora (Annonaceae), popularly known as ‘laranjinha’, is distributed in the Amazon Rainforest, and is mainly found in Brazil, Bolivia, Colombia, Ecuador, Peru, Suriname and Venezuela (GBIF, 2019). There are few reports of the popular use of this plant; however, communities in the interior of the Amazon often use its leaves to make a relaxing tea. Previous phytochemical investigation of this species has described it as having a rich isoquinoline alkaloid content with antiplasmodial and antibacterial activities (Rabelo et al., 2014) but, despite this, there are no published data on the chemical composition of the EO of G. citriodora. Nevertheless, the phytochemical composition of EOs of some species belonging to the genus Guatteria has revealed certain bioactive properties. Guatteria EOs have shown a predominance of oxygenated sesquiterpenoids with biological activities associated to anticancer (Branches et al., 2019, Costa et al., 2020), antileishmanial (Siqueira et al., 2015) and antimicrobial (Alcântara et al., 2017) properties.
Another important aspect, highlighted here, is how the selected molecule acts on a membrane-active mechanism to strengthen its effects against microorganisms. In this study, the results obtained are discussed following the current context of our knowledge regarding the effects of essential oils in relation to morphological alterations to fungal cell structures, as published in Pimentel et al. (2018) and Souza et al. (2020). Herein, it was hypothesized that GcEO induces the leakage of cellular components of microorganisms (fungi), which may lead to structural and/or functional alterations. As such, the aim of this study was to investigate the chemical composition and the antimicrobial potential of essential oil from leaves of G. citriodora, as well as identify the possible antifungal mechanism associated with the morphophysiological alterations.
Section snippets
Information on the origin of the material
The leaves from thirty matrices of G. citriodora were randomly collected in 2019 and 2020 from the Adolpho Ducke Forest Reserve (2° 48′ 72″ S, 59° 53′ 32″ W), Manaus, Amazonas, Brazil. Authentication of the plant species was carried out by INPA taxonomists via comparison with the original voucher (No. 14 570) deposited in the INPA Herbarium, in Manaus. The collection was performed during the morning (8 am), in the month of March (mean rainfall ≅300 mm month−1). The climate of Manaus is
Chemical analysis
Untargeted metabolomic investigation is the description of the quantitation or/and detection of a large number of metabolites from one or more samples. This strategy, known as top-down or metabolite profile strategy, avoids the need for a preceding detailed hypothesis on a particular set of metabolites and, instead, analyzes the total metabolomic profile in a specific complex sample. This is of paramount importance, since phytochemical approaches need to address complex chemical matrices, and
Conclusions
This study shows that the EO isolated from the leaves of G. citriodora has a complex and differentiated metabolomic profile and demonstrated the presence of the most important classes of compounds, highlighting the oxygenated monoterpenes citronellal and citronellol. In addition, in dose-dependent manner, this study demonstrated antibacterial and antifungal activity of the EO against all the pathogens analyzed. The results obtained herein revealed that GcEO treatment was able to suppress the
Funding
This study was financed in part by the Coordination for the Improvement of Higher-Level Personnel - Brazil (CAPES) - Finance Code 001, Amazonas State Research Support Foundation (FAPEAM, Brazil, 024/2014), the São Paulo Research Foundation (FAPESP, Brazil, grant 2020/03390-8) and by the National Council for Scientific and Technological Development (CNPq, Brazil, 308373/2019-7) for financial support of this study. José F. C. Gonçalves acknowledges the fellowship provided by CNPq.
CRediT authorship contribution statement
DP Souza and JFC Gonçalves: Conceptualization, Methodology, Formal analysis, Investigation, Writing – original draft, Funding acquisition, Supervision. JC de Carvalho, KKG da Silva and AV Fernandes: Methodology, Formal analysis. GO Nascimento, MV Ramos, HHF Koolen, DP Bezerra and AS Santos: Methodology, Data analysis, Writing – original draft. DP Souza, JFC Gonçalves, JC de Carvalho, KKG da Silva, AV Fernandes, MV Ramos, HHF Koolen, DP Bezerra and AS Santos: Final version.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
The authors are grateful to the Ministry of Science, Technology and Innovations/National Institute for Amazonian Research (MCTI/INPA - Brazil), as well as the members of the Laboratory of Physiology and Plant Biochemistry of INPA (INPA-LFBV) for the use of the equipment and infrastructure for the analyses and to the Coordination for the Improvement of Higher Education Personnel (CAPES, project Pro-Amazonia: Biodiversity and Sustainability - 042/2012) and National Council for Scientific and
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