REVIEW
The deep continental subsurface: the dark biosphere
Cristina Escudero
1
&
Mónica Oggerin
1,2
&
Ricardo Amils
1,3
Received: 17 April 2018 / Revised: 8 May 2018 /Accepted: 9 May 2018 /Published online: 30 May 2018
#
Springer International Publishing AG, part of Springer Nature 2018
Abstract
Although information from devoted geomicrobiological drilling studies is limited, it is clear that the results obtained so far call for
a systematic exploration of the deep continental subsurface, similar to what has been accomplished in recent years by the Ocean
Drilling Initiatives. In addition to devoted drillings from the surface, much of the continental subsurface data has been obtained
using different subterranean Bwindows,^ each with their correspondent limitations. In general, the number and diversity of
microorganisms decrease with depth, and the abundance of Bacteria is superior to Archaea. Within Bacteria, the most commonly
detected phyla correspond to Proteobacteria, Actinobacteria, Bacteroidetes, and Firmicutes. Within Archaea, methanogens are
recurrently detected in most analyzed subsurface samples. One of the most controversial topics in the study of subsurface
environments is whether the available energy source is endogenous or partly dependent on products photosynthetically generated
in the subsurface. More information, at better depth resolution, is needed to build up the catalog of deep subsurface microbiota
and the biologically available electron acceptors and donors.
Keywords Deep subsurface drilling
.
Geomicrobiology
.
Dark biosphere
.
SLiME
.
Fluorescence in situ hybridization
The beginning of the deep biosphere study
Although it has been about two centuries since Darwin
predicted the possibility of life in the subsurface (Darwin
1839), it was in 1926 when the first data about life at great
depths were obtained (Bastin et al. 1926). Shortly after-
wards, in the 1930s, microbiological studies on marine
sediments demonstrated the existence of life in the oceanic
subsurface (Zobell 1938;ZoBellandAnderson1936).
However, advances in this field in subsequent years were
limited because of the lack of credibility by the scientific
community (Lipman 1931). In addition, after observing
that the combined effect of low temperatures and high
pressure inhibited the growth of microorganisms in the
ocean depths, the possibility of finding active life in the
deep subsurface was severely questioned (Jannasch et al.
1971). The concept of life at great depths changed radically
in 1979, when Corliss and coworkers revealed that in deep
oceanic hydrothermal vents, animal life sustained by the
chemosynthesis produced by sulfur-oxidizing microorgan-
isms existed in an ecosystem completely independent of
photosynthesis (Corliss et al. 1979). Thanks to this discov-
ery, the study of deep biosphere in the oceanic subsurface
was promoted and included in successful international dril-
ling programs (D’Hondt et al. 2002;Oremlandetal.1982;
Whelan et al. 1986).
However, the study of life in the continental subsurface was
not seriously promoted until years after the discovery of the
great biodiversity in the oceanic subsurface. In 1988, Ghiorse
and Wilson denounced the indifference towards the possible
existence of life in terrestrial subsurface environments
(Ghiorse and Wilson 1988). These authors pointed out that
several studies had detected microorganisms in continental
subterranean locations for decades, but they had been ignored
and questioned due to the high risk of contamination during
the sampling (Lipman 1931). For this reason, development
and use of tracers were key in providing credibility to the
study of life in subsurface environments, since they allow
the control of the main sources of microbiological contamina-
tion during sampling (Kieft 2010).
* Ricardo Amils
ramils@cbm.csic.es
1
Centro de Biología Molecular Severo Ochoa (CBMSO,
CSIC-UAM), Universidad Autónoma de Madrid, Cantoblanco,
28049 Madrid, Spain
2
Present address: Max Planck Institute for Marine Microbiology,
Celsiusstrasse 1, 28359 Bremen, Germany
3
Centro de Astrobiología (CAB, INTA-CSIC), Km5 Carretera de
Ajalvir, 28055 Torrejón de Ardoz, Madrid, Spain
International Microbiology (2018) 21:3–14
https://doi.org/10.1007/s10123-018-0009-y
@Phil_Robichaud
@deepthiw
@JoseServera