Igneous oceanic crust is one of the largest potential habitats for life on earth (Orcutt
et al., 2011), and microbial activity supported by rock-water-microbe reactions in
this environment can impact global biogeochemical cycles (Bach and Edwards, 2003).
However, our understanding of the microbiology of this system, especially the subsurface
“deep biosphere” component of it, has traditionally been limited by sample availability
and quality. Over the past decade, several major international programs (such as the
Center for Dark Energy Biosphere Investigations, the current International Ocean Discovery
Program, and its predecessor Integrated Ocean Drilling Program, and the Deep Carbon
Observatory) have focused on advancing our understanding of life in this cryptic,
yet globally relevant, biosphere. Additionally, many field and laboratory research
programs are examining hydrothermal vent systems—a seafloor expression of seawater
that has been thermally and chemically altered in subseafloor crust—and the microbial
communities supported by these mineral-rich fluids. The papers in this special issue
bring together recent discoveries of microbial presence, diversity, and activity in
these dynamic ocean environments.
Starting at the seafloor where igneous rocks are directly exposed to oxic, bottom
seawater, two papers in this special issue address the microbial diversity (Lee et
al.) and metagenomic characteristics (Singer et al.) of seafloor basalts. Going deeper
below the seafloor where cool, oxic fluids circulate through fractures in the lithosphere,
two papers document the biomass and structure (Jørgensen and Zhao) and metabolic potential
(Zhang et al.) of biofilms on subsurface basalts from the western flank of the Mid-Atlantic
Ridge at a site known as North Pond. A companion project at this same site used a
new in situ spectral imaging tool to assess biofilms and biomass in the crustal subsurface
(Salas et al.). Basalts from the seafloor and this oxic subsurface environment were
used in a survey to assay the magnitude of microbial carbon fixation on basalts, and
to identify microbial groups potentially involved in this process (Orcutt et al.).
Isolation and description of bacteria from the overlying sediment at North Pond provides
a comparison between the crustal microbial communities and those detected in the sediment
lying just above (Russell et al.).
Comparing these oxic and cool subsurface crustal fluids with warmer and anoxic subsurface
crustal fluids from the eastern flank of the Juan de Fuca Ridge, a new nanocalorimetry
approach documents the energy available to subsurface crustal fluid communities (Robador
et al.). These new approaches help to validate theoretical models of energy availability
in the crustal subsurface, such as new work in this special issue on hydrogen production
from water-rock reactions (Bach) and radiolysis (Dzaugis et al.). Finally, new time
series data from a crustal observatory at the Juan de Fuca Ridge flank reveals the
importance of redox conditions and temperature on structuring biofilms forming on
crustal rocks (Baquiran et al.).
The Juan de Fuca Ridge and flank environment are also loci of recent efforts to cultivate
thermophilic organisms. Thermophilic sulfate reducing bacteria were isolated from
deep sediment on the ridge flank influenced by the diffusion of sulfate and heat from
the underlying igneous basement (Fichtel et al.), and multivariate laboratory experiments
were conducted to determine controls on thermophilic sulfate reduction in the hydrothermal
sulfide chimney structures nearer to the ridge axis (Frank et al.). The genomes of
isolates of Thermococcus from the Juan de Fuca were compared to isolates from other
hydrothermal systems to explore thermophile biogeography and adaptation (Price et
al.).
Moving to a more organic-rich hydrothermal setting, two papers in the special issue
explore the microbial residents in the Guaymas Basin in the Gulf of California. A
“hiking guide” of Guaymas documents the connection of surface patterns in microbial
mats to subsurface gradients in temperature and porewater chemistry (Teske et al.).
Honing in on the surface microbial mats, and the resident giant sulfur bacteria therein,
an exploration of genomes from these organisms reveals intriguing hints about their
possible transcriptional regulation mechanisms (MacGregor).
Given that oceanic crust is composed of igneous rocks (e.g., basalt, gabbro, peridotite)
enriched in reduced iron, chemosynthetic iron oxidation received focused attention
in this special issue. The growth of chemoorganotrophic (Sudek et al.) and chemolithoautotrophic
(Henri et al.) iron-oxidizing bacteria in the presence of basalt was investigated
with interdisciplinary approaches. Two studies show the early colonization by marine
Zetaproteobacteria—neutrophilic, microaerophilic iron-oxidizing bacteria—on surfaces
containing reduced iron (Henri et al.; McBeth and Emerson). Zetaproteobacteria also
colonize reduced iron substrates in freshwater systems (McBeth and Emerson), and genomes
of freshwater iron oxidizing bacteria reveal similarities and differences to their
marine cousins (Kato et al.). An exploration of the architecture of the microbial
mats generated by freshwater and marine iron-oxidizing bacteria reveals the ecosystem
structuring performed by these lithotrophs (Chan et al.). Finally, an intense investigation
of the alteration products in active and inactive hydrothermal chimneys reveals diverse
signatures of microbial iron oxidation and reduction (Toner et al.).
Cumulatively, the articles in this special issue serve as a tribute to the late Dr.
Katrina J. Edwards (Figure 1), who was a pioneer and profound champion of studying
microbes that “rust the crust” (Bach and Edwards, 2003; Edwards et al., 2003, 2005,
2011a,b, 2012a,b). As co-author on five of the twenty-two papers in this special issue
(Lee et al.; Salas et al.; Singer et al.; Baquiran et al.; Toner et al.), and an acknowledged
inspiration of several others, Katrina's influence on the field has a lasting legacy.
This legacy is eloquently captured in an award-winning feature length documentary
about the North Pond ocean drilling project (https://vimeo.com/117447690), a long-term
observatory project that Katrina initiated to study deep biosphere crustal microbes
(Edwards et al., 2012c). Her legacy lives on in the various collaborators that continue
to study microbes that rust the crust, as well as in the scientists that passed through
her lab and are now running their own labs, including the editors of this volume.
This special issue volume serves as a foundation for the continued exploration of
the subsurface ocean crust deep biosphere.
Figure 1
Dr. Katrina J. Edwards (1968–2014), a visionary geomicrobiologist who promoted the
study of microbes that “rust the crust,” breaking open a seafloor basalt from the
North Pond study site in 2012. Photograph by Beth Orcutt.
Author contributions
All authors listed have made a substantial, direct and intellectual contribution to
the work, and approved it for publication.
Conflict of interest statement
The authors declare that the research was conducted in the absence of any commercial
or financial relationships that could be construed as a potential conflict of interest.