Investigation of the microbial community composition and functional potential in Namib Desert soils

Abstract

Deserts constitute one-fifth of the Earth’s total surface area and represent one of the harshest environments. Soil microbial communities are considered the dominant ecological drivers of these ecosystems as they are major contributors to several processes that are vital for carbon and nutrient cycling. Changes in precipitation regimes have been shown to alter soil microbial communities by causing shifts in community composition. Therefore, gradients of precipitation have been suggested as good systems to evaluate the impact of precipitation on microbial communities, which is largely unexplored in in desert ecosystems. Using 16S rRNA gene high-throughput sequencing and shotgun metagenome sequencing, the taxonomic composition and functional potential of soil prokaryotic communities across two zones with contrasting precipitation history in the Namib desert was investigated. Alpha-diversity of both taxonomic and functional profiles were not impacted by precipitation across the two zones. However, beta-diversity patterns differed significantly between the two zones. Interestingly, a small set of microbial taxa, many of which were present in low abundance, were responsible for these changes. Altogether, these results indicate that precipitation is an important factor in shaping taxonomic and functional attributes of the arid soil microbiome.

Microbes in soil are known to produce antibiotics as an advantage to compete for nutrients and other limited resources which are used to inhibit the growth of or to kill off their competition. These antibiotic producers encode antibiotic resistance genes that protect them from the molecules they produce. Soil is therefore the most prominent reservoir of resistance genes, harbouring up to 30% of the genes that confer resistance to antibiotics, metals and biocides making up the soil resistome. Many studies have focused on the resistomes of grassland, agricultural and even cold desert soils, however, little is known about the resistome of hot deserts. With the use of shotgun metagenomics, the resistome and the mobilome in Namib Desert soils were identified and characterized. A variety of antibiotic resistance genes (ARGs) (e.g., inhA, katG, rpoB) were detected in low abundance including those that were horizontally acquired (e.g., AAC (3’)). The presence of metal/biocide resistance genes (MRGs) in close proximity to ARGs indicated a potential co-selection of resistance to antibiotics and metals/biocides. A decoupling between bacterial community composition and ARG profiles was identified, most likely attributed to the presence of mobile genetic elements and horizontally acquired ARGs. These results showed that bacterial communities in Namib Desert soils host a number of resistance elements and that horizontal gene transfer, rather than phylogeny, could play an essential role in their dynamics. The One Health concept is a holistic and interdisciplinary approach based on the idea that human and animal health are linked to the health of the environment. The exhaustive use of antibiotics in humans, animal farming and other agricultural practices has resulted in the frequent appearance of antibiotic resistant bacteria in human-impacted habitats. However, antibiotic resistance in less impacted habitats (e.g., Deserts) is not well understood. A more in depth investigation of the acquired ARGs revealed the presence of a clinically significant extended spectrum β-lactamase (TEM-116). This ARG was carried on a ColE1-like plasmid also hosting a metal resistance gene coding for arsenate reductase (arsC). The co-selection of resistance to antibiotics and metals encoded on a single mobile genetic element increases the probability of dissemination of these resistance determinants and the potential selection of multiple resistance mechanisms. In addition to these two resistance genes a P7 entero-bacteriophage was found on the same plasmid. This bacteriophage may represent a new vehicle for the propagation of the gene cluster (Tem-116 and arsC) in these soil communities. These results highlight the importance of less impacted environments in the One Health initiative.