Genome of the Cyanobacterium Microcoleus vaginatusFGP-2, a Photosynthetic Ecosystem Engineer of Arid Land Soil Biocrusts Worldwide

Abstract

The filamentous cyanobacterium Microcoleus vaginatusis found in arid land soils worldwide. The genome of M. vaginatusstrain FGP-2 allows exploration of genes involved in photosynthesis, desiccation tolerance, alkane production, and other features contributing to this organism's ability to function as a major component of biological soil crusts in arid lands.

GENOME ANNOUNCEMENT

Arid lands comprise about 40% of the total Earth land mass, and much of the undisturbed soil surface in arid lands worldwide is colonized by biological soil crusts (biocrusts) (1). Cyanobacteria in the genus Microcoleus, particularly strains of M. vaginatus, are the most abundant in biocrusts worldwide, where they help stabilize the soil surface and contribute significantly to soil carbon inputs (1).

The “improved high-quality draft” (4) genome of M. vaginatusstrain FGP-2, an isolate from a dark, pinnacled crust near Moab, Utah, assembled into 6,698,929 bp distributed across 40 contigs with an average GC content of 46%. Automated gene modeling produced 5,478 genes, of which 64% could be assigned a predicted function. Comparison of M. vaginatusFGP-2 to the marine isolate Microcoleus chthonoplastesPCC 7420 (8) via a modified version of Ortholuge (7) identified only 2,044 orthologs, suggesting considerable divergence and confirming that these two organisms are not closely related (9).

The M. vaginatusdraft genome encodes three nearly identical (98% protein identity) copies of D1, a major target protein in photodamage, which presumably enable M. vaginatusto quickly express and replace photoinactivated D1. Each of the three paralogs encodes a glutamate (Glu) at position 130 instead of glutamine (Gln). In Synechocystissp. strain PCC 6803, the Glu-containing D1 form has been shown to increase phototolerance under high-light conditions (3), and site-directed mutagenesis of D1 Q130E at position 130 (Gln to Glu conversion) ultimately reduces oxidative damage caused by back electron flow in photosystem II (PSII) (5, 11).

Arid land soil microorganisms are subjected to extremes in temperature, salinity, and moisture availability and may accumulate organic compounds as osmoregulatory solutes in response to salt stress and desiccation (10, 12, 13). A gene cluster encoding homologs of maltooligosyltrehalose synthase and maltooligosyltrehalose trehalohydrolase (TreYZ) was identified. These genes may enable M. vaginatusto synthesize trehalose from glycogen (15), which is typical of moderately osmo- tolerant cyanobacteria (12) and agrees with early physiological studies (2). The genome also houses a trehalose synthase homolog, which could be important for either the synthesis or the degradation of trehalose from maltose (15).

Directly downstream of TreYZ are homologs of an acyl-[acyl carrier protein] (ACP) reductase and an aldehyde decarbonylase, the products of which have been experimentally verified to synthesize heptadecane and pentadecane alkanes in multiple cyanobacterial genera (14). This finding is consistent with a previous report indicating that an isolate of M. vaginatusproduces an unusual variety of branched alkanes and apolar carbon compounds, the most dominant being heptadecane (6).

The genome of M. vaginatusFGP-2 constitutes an invaluable tool to understand the unique adaptations that enable microbial colonization of arid environments as well as the potential for generation of alternative biofuels.

Nucleotide sequence accession number.

The sequence and annotation of the draft genome of M. vaginatusFGP-2 is available at GenBank/EMBL/DDBJ under accession number AFJC00000000.