Lechuguilla cave microbiome

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Introduction

Lechuguilla Cave is a deep and expansive cave in New Mexico, USA. The cave and its microbiome have attracted interest from microbiologists because, despite several million years of isolation from the terrestrial environment, bacterial isolates from the cave display widespread resistance to modern clinical antibiotic drugs. This discovery sheds new light on the origin of antibiotic resistance genes, and it offers new opportunities for developing effective next-generation antibiotic drugs.

Geology

Lechuguilla Cave is located in Carlsbad Caverns National Park, New Mexico. It formed between four and seven million years ago through hypogenic speleogenesis [1]. Hydrogen sulfide from hydrocarbons in the nearby Delaware Basin became oxidized to sulfuric acid, and acidified groundwater infiltrated upward into the carbonate rock of the Capitan Formation, thereby forming Lechuguilla Cave [2].

After formation, the aquifer dropped leaving the cave hydrologically isolated from phreatic groundwater. The cave is also hydrologically isolated from above by the impermeable rock of the Yates Formation that overlies the Capitan Formation [3]. As a result, the influx of terrestrial water occurs very slowly and in negligible quantities. The cave and its biota have remained effectively isolated from the terrestrial environment and human activity. Water infiltrating into the cave today would have left the surface long before the advent of human antibiotic use in agriculture and medicine [4].

Cave Environment and Biodiversity

Lechuguilla Cave is an extreme environment defined by darkness and limited nutrients. Nonetheless, diverse microbial communities inhabit the aphotic and oligotrophic surfaces of the cave in rich biofilms. These communities are anchored by chemolithoautotrophic primary producers who oxidize ferromanganese substances in the rock, leaving distinctive deposits of ferromanganese ores nearby [5]. These chemolithoautotrophs support secondary populations of chemoheterotrophic bacteria, archaea, and fungi [6].

Figure 1: Red-brown and brown ferromanganese deposits from survey site in Lechuguilla Cave [7]. Close-up shows scale (cm) and texture of deposits

Several fungal and bacterial phyla have been isolated from the cave. These include the fungi Penicillium, Aspergillus, Cylindrocladium, Rhizopus, Mycelia sterilia, Mucor, Paecileomyces, Fusarium, and Epicoccum; and the bacteria Bacillus, Actinomycetes, Arthrobacter, Chryseomonas luteola, Rhodococcus, and Staphylococcus [8].

Microbial Ecology

The extreme oligotrophic nature of the cave environment means that interactions within these microbial communities are defined by fierce competition over scarce nutrients and complex cooperation to make the most of whatever is consumed [9]. Both processes of competition and cooperation are mediated by secondary metabolite products, specifically those with antibiotic properties [10]. The antagonistic use of these antibiotic metabolites has been well researched. Many bacteria and fungi are known to secrete metabolities with antimicrobial activity to inhibit growth by competitors [11]. Indeed, almost all clinical antibiotic drugs are derived from natural metabolites, many of which are produced by terrestrial members of the phyla found in Lechuguilla Cave [12].

But new research suggests that these metabolites are not only used for competitive purposes; they have also been implicated in the cooperative process of biofilm formation as signaling molecules [13]. Researchers at the University of British Columbia, Canada have demonstrated that these metabolites are often present in the environment in concentrations far below their minimum inhibitory concentration, suggesting additional functions beyond antimicrobial competition http://en.wikipedia.org/wiki/Biofilm#Extracellular_matrix. This research also found that growth in the presence of low concentrations of these metabolites can significantly alter transcriptional activity, suggesting that at low concentrations these metabolites act as signaling molecules [15].

The extensive use of these metabolites to mediate biofilm formation is not surprising in an extreme environment like Lechuguilla Cave. Biofilms engender cooperation within the microbial community. The exopolysaccharide matrix of the biofilm inhibits the diffusion of toxic compounds from the surroundings, facilitates the absorption of nutrients, protects the community from desiccation and other environmental factors, and promotes the exchange of genetic material so that adaptation to the habitat can be accelerated [16]. Biofilms confer a significant survival advantage to microbial communities living in extreme conditions.


References