The genome of Bacillus coahuilensis reveals adaptations essential for survival in the relic of an ancient marine environment

Abstract

The Cuatro Cié negas Basin (CCB) in the central part of the Chihuahan desert (Coahuila, Mexico) hosts a wide diversity of microorganisms contained within springs thought to be geomorphological relics of an ancient sea. A major question remaining to be answered is whether bacteria from CCB are ancient marine bacteria that adapted to an oligotrophic system poor in NaCl, rich in sulfates, and with extremely low phosphorus levels (<0.3 M). Here, we report the complete genome sequence of Bacillus coahuilensis, a sporulating bacterium isolated from the water column of a desiccation lagoon in CCB. At 3.35 Megabases this is the smallest genome sequenced to date of a Bacillus species and provides insights into the origin, evolution, and adaptation of B. coahuilensis to the CCB environment. We propose that the size and complexity of the B. coahuilensis genome reflects the adaptation of an ancient marine bacterium to a novel environment, providing support to a ''marine isolation origin hypothesis'' that is consistent with the geology of CCB. This genomic adaptation includes the acquisition through horizontal gene transfer of genes involved in phosphorous utilization efficiency and adaptation to high-light environments. The B. coahuilensis genome sequence also revealed important ecological features of the bacterial community in CCB and offers opportunities for a unique glimpse of a microbe-dominated world last seen in the Precambrian.evolution ͉ genomic adaptation ͉ horizontal gene transfer ͉ phosphorus stress ͉ sulfolipids T he Cuatro Ciénegas Basin (CCB) is located in a valley Ϸ740 m above sea level in the state of Coahuila, Mexico, that measures Ϸ30 km by 40 km and is surrounded by high mountains (Ͼ3,000 m) (Fig. 1). CCB is an enclosed evaporitic basin that receives Ϸ150 mm of annual precipitation. Despite the dry climate of the valley, the CCB harbors an extensive system of springs, streams, and pools (1). The CCB ecosystem is not only characterized by a high endemism of macrooganisms and biodiversity of microorganisms (1, 2), but also by extremely oligotrophic waters that are unable to sustain algal growth, making microbial mats the base of the food web (3). In particular, phosphorus (P) levels in CCB appear to be rather low, because they were below the level of detection of several methods used (0.3 M) and the extremely high biomass C:P and N:P ratios (Ͼ100 by moles) previously reported for CCB stromatolites (3, 4). Unlike the present sea, the Churince spring water is poor in NaCl and carbonates, but it is rich in sulfates, magnesium, and calcium (4). Characterization of the microbiological diversity by sequencing 16S rRNA genes revealed that nearly half of the phylotypes from the CCB were closely related to bacteria from marine environments (2). Bacillus coahuilensis is a free-living, spore-forming bacteria isolated from the water column of a shallow desiccation lagoon in the Churince system at CCB (4) (Fig. 1 A and B). A molecular phylogenetic analysis of 16S rRNA sequences indicates that B. coahuilensis is closely ...

How To Live with Phosphorus Scarcity in Soil and Sediment: Lessons from Bacteria

“…For instance, Bacillus coahuilensis, isolated from the Churince Pond in Cuatro Ciénegas, Coahuila, Mexico, was shown to have unique features compared to most well-studied Bacillus spp., such as having a small genome, lacking teichoic acid (a P-rich cell wall component), and having the capability to synthesize membrane sulfolipids in addition to phospholipids (26).…”

Genomics of Bacteria from an Ancient Marine Origin: Clues to Survival in an Oligotrophic Environment

“…For example, all of the twocomponent (histidine-kinases) as well as the unusual sensitive rhodopsins, such as in the case of B. coahuilensis, were found to be overrepresented, indicating that most of the responses of the bacteria that have had their genomes analyzed are environmentallytriggered when compared to generalist and cosmopolitan organisms, such as B. subtilis. Moreover, these comparisons also showed an underrepresentation of secondary metabolism genes in the genome of B. coahuilensis (Alcaraz et al 2010;Alcaraz et al 2008;Desnues et al 2008) (Fig. 4).…”

“…Systematic studies have also been used to describe new species of bacteria using current criteria (Anderson et al 2005;Cerritos et al 2008;Ehling-Schulz et al 2005;Escalante et al 2009;Helgason et al 2004) as well as by attempting to apply multivariate analysis and physical-chemical analyses in order to determine special relationships amongst the bacteria (Cerritos et al 2011). At the genomic scale, 2 genomes (Alcaraz et al 2010;Alcaraz et al 2008) and 3 metagenomes (Breitbart et al 2009;Desnues et al 2008;Dinsdale et al 2008) had been described, in which genes that allow for adaptation to the oligotrophic environment of Cuatro Cienegas have been identified. Two additional metagenomes from microbial mats and several more microbial genomes are currently under analysis.…”

“…Thus, the high diversity of CCB would be a product of two things: the diversity already present at the time of isolation, and the new community assemblages that arose in this unique aquatic environment Souza et al 2006). Firmicutes, an abundant and widespread genera within CCB (Alcaraz et al 2010;Alcaraz et al 2008;Cerritos et al 2011;Moreno-Letelier et al 2011;Souza et al 2006) are the focal group of our studies, in part because there are several endemic species within the site, and because the whole genome has been sequenced for both Exiguobacterium and Bacillus isolates (Bacillus coahuilensis m4-4 ; Bacillus sp. m3-13 (Alcaraz et al 2010); and several unpublished data (from drafts Bacillus sp.…”

First Draft Genome Sequence of a Strain from the Genus Citricoccus

“…Here we present the draft genome sequence of Citricoccus strain CH26A, isolated from the Cuatro Ciénegas Basin (CCB) in Coahuila, Mexico. The CCB is a system of subterranean water streams and ponds characterized by high endemism and biodiversity of macro-and microorganisms and an extremely oligotrophic aquatic environment, poor in NaCl and carbonates and rich in magnesium, calcium, and sulfates (1). Therefore, analysis of the CH26A genome would help us to gain insight into the evolution and adaptation of the actinomycete metabolism to the CCB.…”