Metatranscriptomic characterization of the bacterial community of a contaminated mangrove from the Caribbean
Graphical abstract
Introduction
Microorganisms in the mangrove constitute a large collection of metabolic pathways with biotechnological potential and environmental applications (Gomes et al., 2011). These microorganisms are responsible for organic matter transformation, nutrient cycling (Holguin et al., 2001), synthesis of enzymes of biotechnological interest (Gonçalves et al., 2015, Li et al., 2012), xenobiotic biodegradation (Cabral et al., 2019), and synthesis of antimicrobial compounds, among others (Arumugam and Senthil Kumar, 2017). Microbial communities in mangroves have been evaluated through different approaches, since culture-dependent techniques to omic strategies. Through metagenomics has been established the taxonomic and functional diversity of microorganisms in different mangroves (Alzubaidy et al., 2016, Andreote et al., 2012, Ceccon et al., 2019, Jiang et al., 2013, Lin et al., 2019, Thompson et al., 2013, Zhang et al., 2018). However, the metagenomics does not represent the metabolically active community (Bailly et al., 2007), which triggers differential responses to a disturbance such as pollution (Cabral et al., 2018).
Few studies have been focused on gene expression of the bacterial communities of mangrove (Cabral et al., 2018, Cotta et al., 2019, Rampadarath et al., 2018), in part due to the technical difficulties of extracting good quality RNA from this type of samples rich in organic matter, clays, and tannins (Moran, 2009). These studies have reported that mangrove microorganisms are affected at the taxonomic level by disturbances caused by anthropogenic activity, while high functional redundancy prevails due to their ability to cope with pollution (Cabral et al., 2018), and maintain the balance of the ecosystem. The microbial response to long-term anthropogenic impact in two altered mangroves and one pristine mangrove soils from Brazil (Cabral et al., 2018). Similarly, Cabral et al. (2016) evaluated the activity of microbial genes in heavy metals and antibiotic resistome in the microbial community associated with mangroves in Brazil. Microbial gene expression related to biogeochemical cycles on the coast of Mauritius in natural and artificial mangroves has also been evaluated (Rampadarath et al., 2018). For the Caribbean, no metatranscriptomic works of mangrove microorganisms were found.
Our objective was to characterize the metatranscriptome of a polluted mangrove at the taxonomic level, the cycle of nutrients such as nitrogen, sulfur and methane, and xenobiotic degradation. In this mangrove have been reported human pathogenic bacteria such as Bacillus spp., Micrococcus spp., Staphylococcus spp., Alcaligenes spp., Stenotrophomonas spp, Pseudomonas fluorescens, and Chromobacterium violaceum from wastewater (López et al., 2009). This type of pollutant can influence the structural and functional composition of microbial communities (Gomes et al., 2011, Zhou et al., 2008). We hypothesize that in the metatranscriptome of a disturbed mangrove, few taxonomic groups should prevail in high abundances, and thus the mangrove ecosystem services be affected. Previously, we detected 21 pathways and 193 genes associated with the degradation of xenobiotics in these mangroves (Muñoz García et al., 2019) and reported biomarkers of contamination (Torres et al., 2019). However, in many of these degradation pathways were not detected all the genes associated with the process. Therefore, metatranscriptomics can be a complementary tool to understand how mangrove microorganisms respond to a constant disturbance such as the entry of wastewater into the ecosystem.
Section snippets
Sample collection
Three soil samples were collected from a mangrove located in Valle de Los Cangrejos in La Guajira, Colombia, which is in an altered state, due to wastewater pollution and the proximity to a vehicular dock (1133’28.6”N - 7253’15.0”W). This mangrove has low tree density and high concentration of pollution indicators such as nitrates (527 g/L), phosphates (159 g/L), and dissolved petroleum hydrocarbons and dispersed equivalents of chrysene (8.45 g/L) (INVEMAR, 2017). The samples were kept in
Results
All the analyzed samples represent biological replicates for the same sampling spot. The physical and chemical characteristics of the rhizospheric soil are presented in Table 1. The count of raw reads for the three samples was 60,718,935. The transcriptome for two samples was represented for approximately 24 million raw reads, and one sample had 12.6 million reads (Figure S1). For the functional and taxonomic characterization, we obtained 9,695,735 of the clean reads had at least one hit with
Discussion
We characterize the metatranscriptome of a mangrove influenced by wastewater to level taxonomic, nutrient cycle, and xenobiotic degradation, located on the Caribbean coast of Colombia (La Guajira). The marked dominance of a few taxonomic categories in the expression of the microbial communities of the mangroves suggests a disturbed environment (Ager et al., 2010) (Fig. 1, Fig. 2). In undisturbed natural environments, microbial communities would be rich in species and an abundance of highly
Conclusion
Through a metatranscriptomic analysis, the taxonomic and functional potential of the microorganisms in a mangrove affected by wastewater was reconstructed. The predominance of few taxonomic groups suggests an altered mangrove; however, the functional potential of the mangrove is consistent with that reported for mangroves, which indicates that the few prevalent taxonomic groups are capable of responding metabolically and maintaining resilience in the ecosystem despite environmental
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
This work was funded by COLCIENCIAS, Universidad Antonio Nariño, and Universidad Nacional de Colombia , Medellín headquarters through the project with code FP44842-529-2014 in the call 659-2014 and supported by the postdoctoral fellowship of Colciencias 784–2017.
Nucleotide Sequence Accession Numbers
The access numbers for the data set will be provided at the time of acceptance of the manuscript for publication.
Compliance with Ethical Standards
Additional informed consent was obtained from all
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