Drop-size soda lakes: transient microbial habitats on a salt-secreting desert tree

Abstract

We describe a hitherto unrecognized bacterial community, inhabiting the leaf surfaces of the salt-excreting desert tree Tamarix. High temperatures, strong radiation, and very low humidity dictate a daytime existence in complete desiccation, but damp nights allow the microbial population to proliferate in a sugar-rich, alkaline, and hypersaline solution, before drying up again after sunrise. The exclusively bacterial population contains many undescribed species and genera, but nevertheless appears to be characterized by relatively limited species diversity. Sequences of 16S rRNA genes from either isolates or total community DNA place the identified members of the community in five bacterial groups (Actinobacteria, Bacteroidetes, Firmicutes, alpha-, and gamma-Proteobacteria); in each of these, they concentrate in a very narrow branch that in most cases harbors organisms isolated from unrelated halophilic environments.

Figure 1.—

A Tamarix aphylla leaf. (A) Early morning, dew-covered branches; (B) cross section emphasizing NaCl encrustation; (C) scanning electron micrograph of two adjoining stem segments; (D) environmental scanning electron micrograph of a bacterial microcolony on a leaf surface following several hours' incubation in a humid environment.

Figure 2.—

Numbers of identified (closest relatives) genera of Tamarix phyllosphere bacteria; red, isolates growing on solid media; yellow, 16S rRNA gene sequences from DGGE gels; blue, 16S rRNA gene sequences from clone libraries.

Figure 3.—

A general phylogenetic tree (constructed using ARB) of the Bacteria domain, highlighting the branches where Tamarix sequences congregate. Phyla are marked in blue; the five phyla harboring Tamarix representatives were expanded to the order level, and the orders inhabited by these representatives were marked in red. For detailed phylogenetic trees of the five phyla see supplemental Figures 1–5.

Figure 4.—

Diversity estimates of phyllosphere bacterial populations based on OTUs derived from 16S rRNA gene clone libraries and on amplified ribosomal DNA restriction analysis patterns.