Comparative metagenomics of two microbial mats at Cuatro Ciénegas Basin I: ancient lessons on how to cope with an environment under severe nutrient stress

Abstract

The Cuatro Ciénegas Basin (CCB) is an oasis in the desert of Mexico characterized by low phosphorus availability and by its great diversity of microbial mats. We compared the metagenomes of two aquatic microbial mats from the CCB with different nutrient limitations. We observed that the red mat was P-limited and dominated by Pseudomonas, while the green mat was N-limited and had higher species richness, with Proteobacteria and Cyanobacteria as the most abundant phyla. From their gene content, we deduced that both mats were very metabolically diverse despite their use of different strategies to cope with their respective environments. The red mat was found to be mostly heterotrophic, while the green mat was more autotrophic. The red mat had a higher number of transporters in general, including transporters of cellobiose and osmoprotectants. We suggest that generalists with plastic genomes dominate the red mat, while specialists with minimal genomes dominate the green mat. Nutrient limitation was a common scenario on the early planet; despite this, biogeochemical cycles were performed, and as a result the planet changed. The metagenomes of microbial mats from the CCB show the different strategies a community can use to cope with oligotrophy and persist.

FIG. 1.

Frequency of reads corresponding to gene markers for biochemical cycles. Red mat is shown in red bars while green mat is shown in green bars. Genes correspond to the following proteins: phnD and ptxB (phosphonate transporters), phnH and htxB (C-P lyase), ppA (pyrophosphatase), ppK (polyphosphatase kinase), ppX (exopolyphosphatase), phoA and phoX (alkaline phosphatases), pstS (phosphate transporter), rbcL and rbcS (RuBisCO), codH (CO dehydrogenase), aclY (citrate lyase), nifH (nitrogenase reductase), nrfA (nitrite reductase), narG (nitrate reductase), napA (nitrate reductase), narB (nitrate reductase), nirS (nitrite reductase), norB (nitric oxide reductase), and nosZ (nitrous oxide reductase). Color images available online at www.liebertpub.com/ast

FIG. 2.

Functional comparison of metagenomes from aquatic microbiomes by PCA analysis of SEED Subsystems level 1 (Meyer et al., 2008). Stromatolites PA and RM (Breitbart et al., 2009), Global Ocean Sampling (GOS) (Rusch et al., 2007), Guerrero Negro hypersaline mat (Kunin et al., 2008). The correlation of each variable with factor 1 is available as Supplementary Material, Table S2. Color images available online at www.liebertonline.com/ast