Insights into the response of mangrove sediment microbiomes to heavy metal pollution: Ecological risk assessment and metagenomics perspectives

Rapid urbanisation and ensuing anthropogenic pollution lead to an escalated occurrence of heavy metals and metal-resistant bacteria in the soil ecosystem. Mangrove ecosystems are particularly vulnerable to heavy metal bioaccumulation and often act as metal sinks of the coastal areas. As a consequence, the microbial population in mangrove sediments develop multifarious metal tolerance mechanisms to combat metal toxicity. In this context, metagenomic investigation of two mangroves, viz. Mangalavanam and Puthuvypin from the heavily populated metropolitan city, Cochin (Central Kerala, India) was undertaken to discern the metal resistance functions and taxonomic diversity of the microbial consortia. Estimation of heavy metal content using Inductively Coupled Plasma Atomic Emission Spectrometer (ICP-MS) identified the abundance of zinc, chromium, nickel copper, lead, arsenic, and cadmium in the mangrove sediments. Ecological risk index values indicated high cadmium contamination of the two estuarine samples. Whole metagenome shotgun sequencing of the Central Kerala mangroves and comparative analysis with mangrove metal resistomes from other geographical regions revealed the prevalence of cobalt-zinc-cadmium resistance and preponderance of Proteobacteria in all the datasets. Cation efflux system protein CusA constituted the majority of the reads at the function level. Comparative analysis of taxonomy identified the dominance of Anaeromyxobacter, Geobacter, Pseudomonas, Candidatus Solibacter, and Pelobacter in the mangrove datasets. Non-metric multidimensional scaling analysis of the metal resistance genes depicted strong geographical clustering of the function and composition of metal resistant bacteria, suggesting a strong innate resilience of microbiome towards anthropogenic perturbations. More robust studies with intensive sampling will enhance our understanding of the occurrence, interactions, and functions of microbial heavy metal resistome in mangrove ecosystems.