Genomic comparisons of a bacterial lineage that inhabits both marine and terrestrial deep subsurface systems

Sean P. Jungbluth,Susannah G. Tringe,Tijana Glavina del Rio,Michael S. Rappé,Ramunas Stepanauskas

doi:10.7717/peerj.3134

Abstract

It is generally accepted that diverse, poorly characterized microorganisms reside deep within Earth’s crust. One such lineage of deep subsurface-dwelling bacteria is an uncultivated member of the Firmicutes phylum that can dominate molecular surveys from both marine and continental rock fracture fluids, sometimes forming the sole member of a single-species microbiome. Here, we reconstructed a genome from basalt-hosted fluids of the deep subseafloor along the eastern Juan de Fuca Ridge flank and used a phylogenomic analysis to show that, despite vast differences in geographic origin and habitat, it forms a monophyletic clade with the terrestrial deep subsurface genome of “Candidatus Desulforudis audaxviator” MP104C. While a limited number of differences were observed between the marine genome of “Candidatus Desulfopertinax cowenii” modA32 and its terrestrial relative that may be of potential adaptive importance, here it is revealed that the two are remarkably similar thermophiles possessing the genetic capacity for motility, sporulation, hydrogenotrophy, chemoorganotrophy, dissimilatory sulfate reduction, and the ability to fix inorganic carbon via the Wood-Ljungdahl pathway for chemoautotrophic growth. Our results provide insights into the genetic repertoire within marine and terrestrial members of a bacterial lineage that is widespread in the global deep subsurface biosphere, and provides a natural means to investigate adaptations specific to these two environments.

Highlights

Recent progress in understanding the nature of microbial life inhabiting the sedimentburied oceanic crust has been made through the use of ocean drilling program borehole observatories as platforms to successfully sample fluids that percolate through the subseafloor basement (Wheat et al, 2011)
Following subsequent screening and removal of contaminating sequences (Table S4), six genomic scaffolds from U1362A totaling 1,778,734 base pairs in length and originating from only the U1362A metagenome were identified that correspond to the draft ‘‘Ca. D. cowenii’’ modA32 genome described here (Table 1)
This study takes advantage of new sampling technologies and couples them with improvements to DNA sequencing and associated informatics tools in order to reconstruct the genome of an uncultivated Firmicutes bacterium from fluids collected deep within the subseafloor of the Juan de Fuca Ridge flank that has previously been documented within both the terrestrial and marine subsurface

Summary

Introduction

Recent progress in understanding the nature of microbial life inhabiting the sedimentburied oceanic crust has been made through the use of ocean drilling program borehole observatories as platforms to successfully sample fluids that percolate through the subseafloor basement (Wheat et al, 2011). Ribosomal RNA (16S rRNA) gene cloning and sequencing from the crustal fluids led to the first confirmation of microbial life in the deep marine igneous basement and revealed the presence of diverse bacteria and archaea. Discovered in this initial survey was an abundant, uniquely branching lineage within the bacterial phylum Firmicutes that was only distantly related to its closest known relative at the time, a thermophilic nitrate-reducing chemoautotroph isolated from a terrestrial volcanic hot spring, Ammonifex degensii (Huber et al, 1996). Based on 16S ribosomal RNA sequence analyses, most of the terrestrial and marine lineages form a monophyletic clade of predominantly subsurface origin but do not partition into subclades of exclusively terrestrial and marine origin, suggesting that there may have been multiple transitions between the terrestrial and marine deep subsurface environments (Jungbluth et al, 2013)

Methods

Results

Conclusion