An endangered oasis of aquatic microbial biodiversity in the Chihuahuan desert

Abstract

The Cuatro Cienegas basin in the Chihuahuan desert is a system of springs, streams, and pools. These ecosystems support >70 endemic species and abundant living stromatolites and other microbial communities, representing a desert oasis of high biodiversity. Here, we combine data from molecular microbiology and geology to document the microbial biodiversity of this unique environment. Ten water samples from locations within the Cuatro Cienegas basin and two neighboring valleys as well as three samples of wet sediments were analyzed. The phylogeny of prokaryotic populations in the samples was determined by characterizing cultured organisms and by PCR amplification and sequencing of 16S rRNA genes from total community DNA. The composition of microbial communities was also assessed by determining profiles of terminal restriction site polymorphisms of 16S rRNA genes in total community DNA. There were 250 different phylotypes among the 350 cultivated strains. Ninety-eight partial 16S rRNA gene sequences were obtained and classified. The clones represented 38 unique phylotypes from ten major lineages of Bacteria and one of Archaea. Unexpectedly, 50% of the phylotypes were most closely related to marine taxa, even though these environments have not been in contact with the ocean for tens of millions of years. Furthermore, terminal restriction site polymorphism profiles and geological data suggest that the aquatic ecosystems of Cuatro Cienegas are hydrologically interconnected with adjacent valleys recently targeted for agricultural intensification. The findings underscore the conservation value of desert aquatic ecosystems and the urgent need for study and preservation of freshwater microbial communities.

Fig. 1.

Molecular data from rRNA gene sequences in samples from the region of Cuatro Cienegas. (A) Proportion of habitat affiliations of the sequences based on comparison of our 16S rRNA clone library sequences with the Ribosomal Database Project. The large pie diagram illustrates the habitat affiliations for all of the samples, and the smaller diagrams indicate the distributions for each of the sampled valleys. The meaning of each color in the diagrams is shown to the right of the total sample. (B) The phylogenetic tree for microorganisms of the CCB was obtained as a maximum-parsimony tree with 1,000 bootstraps of the 690-bp common fragment of the 16S rRNA gene sequences. The bootstrap value is shown in the branches; none of the bootstrap values is <86%. The symbols show the sampling site for each sequence, and the color of each sequence shows its habitat affiliation (dark blue for marine, light blue for fresh water, brown for soils and sediments, and red for hydrothermal- and magma-associated taxa).

Fig. 2.

Habitat affiliation was tested with a nearest-neighbor analysis, where each cloned sequence was compared with those reported for the most closely related reference sequences in gene sequence databases. The habitat of origin of the reference sequence was assigned to the undescribed population from eight studies from the literature (17, 29, 35, 40–44) as well as our study. Microbial samples were from the following habitats: CCB (springs and deep water from Cuatro Cienegas Coahuila); sulfurous lakes (Cisó and Valar lakes, Spain); saline Atacama lake (a lake in Atacama desert, Northern Chile); saline Mono Lake (California); soil (soils of the arid southwestern United States); Changjiang River (China); a subterranean river (Sulfur River, Parker Cave, Kentucky); sea (marine waters of the Cariaco Basin, Pacific Ocean); hypersaline lakes (Antarctica); and freshwater (water in a drinking water distribution system) (More data available in Table 4).