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surrounding crust must be weak, with only a
few exceptions. Stresses are likely no higher
than a few tens of MPa, rather than hundreds of MPa expected from standard friction theory. Apparently, not that much stress
is required to make a great earthquake fault
slip, and when it does, it drops the ambient
stress to extremely low levels.
Hardebeck suggests that most faults in
the world’s subduction zones are weak.
What might produce such weakness? Possible explanations include intrinsically low
friction of fault zone materials composed of
clays and talc (11), high fluid pressures that
push against the normal stress on faults
(10), and dynamic shear weakening during
earthquake fault slip (12). It is important
to remember that the inference of stress
is indirect and depends on the accuracy
of the fault plane orientations and various
assumptions made when inferring stress
orientations from the fault slip data. To improve our knowledge of the magnitude and orientation of stress in
Stress axes
subduction zones and the factors
determining their variations in
space and time, we need muchWeak
improved observations. More
megathrust
detailed observations of small
Weak crust
earthquakes and their fault plane
orientations near the megathrust
on
require seafloor seismic sensors.
cti
u
bd
Seafloor geodetic measurements
Su
can capture the strain associated
with evolving stress (13). Improved
Weak subduction zones. The orientation of compressive stress
in situ observations are possible
inferred from the geometry of many small earthquake fault planes
by drilling into a megathrust at
suggests a weak megathrust in a weak surrounding crust.
greater depths to directly observe
the composition, stress, and condiwe would expect the principal stresses to
tions in the fault zone (14). The distribube nearly perpendicular and aligned with
tion of absolute stress in space and time
the fault, similar to the case for the free
is probably the most important quantity
Earth’s surface. If both the megathrust and
in solid earth sciences that we know the
surrounding material are either weak or
least about. The analysis reported in Hardstrong, we would expect the maximum comebeck’s paper takes an important step topressive stress to be oriented at an oblique
ward changing that. ■
angle (20° to 60°) from the fault.
REFERENCES
Contrary to expectations, Hardebeck finds
1. J. Hardebeck, Science 349, 1213 (2015).
that the orientation of maximum compres2. E. M. Anderson, The Dynamics of Faulting and Dyke
sive stress near most subduction thrusts
Formation with Application to Britain (Oliver & Boyd,
Edinburgh, 1951).
plunges toward the trench at angles of 10°
3. J. Byerlee, Pure Appl. Geophys. 116, 615 (1978).
to 50°. This indicates that the state of stress
4. M. Brudy, M. D. Zoback, K. Fuchs, F. Rummel, J.
is not Andersonian and that the maximum
Baumgärtner, J. Geophys. Res. 102, 18453 (1997).
5. P. M. Fulton et al., Science 342, 1214 (2013).
compressive stress is oriented roughly 30°
6. X. Gao, K. Wang, Science 345, 1038 (2014).
from the megathrust. This orientation is
7. M. E. Magee, M. D. Zoback, Geology 21, 809 (1993).
expected for faults with frictional strength
8. A. Hasegawa, K. Yoshida, T. Okada, Earth Planets Space 63,
703 (2011).
similar to that of the surrounding crust;
9. J. Hardebeck, Geophys. Res. Lett. 39, 21313 (2012).
that is, they are either both strong or both
10. P. Audet et al., Nature 457, 76 (2009).
weak. Using evidence of absolute megathrust
11. D. E. Moore, M. J. Rymer, Nature 448, 795 (2007).
12. G. Di Toro et al., Nature 471, 494 (2011).
weakness from studies documenting low
13. R. Bürgmann, C. D. Chadwell, Annu. Rev. Earth Planet. Sci.
frictional heat production (5, 6), stress ro42, 509 (2014).
tations due to great earthquakes (8, 9), and
14. W. Lin et al., Science 339, 687 (2013).
high fluid pressures in fault zones (10), Hardebeck argues that both the megathrust and
10.1126/science.aac9625
SCIENCE sciencemag.org
EVOLUTION
How single
cells work
together
Are single-celled
symbioses organelle
evolution in action?
By Jonathan P. Zehr
S
ymbiotic interactions are fundamental to life on Earth and were critical
for the evolution of organelles that
led to the success of eukaryotes on
the planet. Such mutualistic interactions between unicellular microorganisms and multicellular plants and
animals are pervasive in natural and agricultural ecosystems (1). In contrast, very
little is known about symbiotic interactions
between unicellular partners. Recent studies have revealed single-celled nitrogenfixing symbioses that require different
mechanisms to maintain symbiosis than
seen in multicellular systems.
In aquatic environments, there are many
examples of protists that acquire endosymbionts or plastids (2). These types of
symbioses are analogous to the evolution
of organelles, such as the photosynthetic
organelle of the unicellular eukaryote Paulinella (3). Other unicellular mutualistic
associations are nitrogen-fixing symbioses—
for example, between filamentous cyanobacteria and marine diatoms (see the figure,
panel A) (4). The filamentous cyanobacteria
in these associations develop specialized
cells (heterocysts) that allow them to separate the oxygen generated by photosynthesis
from the oxygen-sensitive nitrogen fixation
enzymes. In these symbioses, the intracellular cyanobacteria coordinate growth and
division and are transmitted through different life stages (5). More recent studies have
found evidence for nitrogen-fixing symbioses between unicellular cyanobacteria and
single-celled protists that do not involve the
development of specialized cells.
One example is a nitrogen-fixing symbiosis between the single-celled cyanobacterium UCYN-A (unicellular cyanobacteria
nitrogen-fixing “group A”) and a prymnesiophyte microalga (see the figure, panel B)
Department of Ocean Sciences, University of California, Santa
Cruz, Santa Cruz, CA 95064, USA. E-mail: [email protected]
11 SEP TEMBER 2015 • VOL 349 ISSUE 6253
Published by AAAS
1163
Downloaded from www.sciencemag.org on September 11, 2015
of geophysical studies in some subduction
zones have suggested that fault friction values and stress may be much lower than expected from laboratory experiments. Such
studies have relied on estimates of frictional
heat generated by faulting (5, 6), the orientation of stresses estimated from the geometry of aftershock fault planes (7), as well
as the apparent large rotation in principal
stress orientations from before to after the
2011 Tohoku earthquake in Japan (8, 9).
Hardebeck focuses on using the fault
plane geometry of small earthquakes near
and above the megathrust of global subduction zones to determine the orientations of
the principal stresses and constrain their
magnitudes. The orientation of the maximum principal stress with respect to the
megathrust provides information about
the relative strength of the fault and surrounding crust. If the megathrust is weak
(low friction) in an otherwise strong crust,
(6, 7). This symbiosis is one of a few documented symbioses with a prymnesiophyte
(a group of protists) and the only known nitrogen-fixing symbiosis with a haptophyte.
Furthermore, the nitrogen-fixing cyanobacterial partner exhibits dramatic genomic reductions that have led to a very high degree
of metabolic streamlining (8). A second
in the sense that they evolved within the
cyanobacteria lineage.
These single-celled symbioses are intriguing models of nitrogen-fixing symbiosis in general, but are perhaps even more
interesting as models of the evolutionary
events that led to eukaryotic organelles.
The genome reduction implies that the
cyanobacterium must be obligate and implies an evolutionA
ary “luggage” strategy of the
host (11), because it must always
carry the symbiont even if is not
physiologically advantageous at
all times.
It is curious that these single-celled symbioses did not
ultimately give rise to a nitro100 µm
gen-fixing organelle, given the
B
importance of nitrogen as a nutrient that limits the productivity
of terrestrial and aquatic ecosystems. The unicellular cyanobacterial symbiotic partners are as
close to being such nitroplasts
as anything yet known. Indeed,
some features of the UCYN-A
1 µm
1 µm
reduced genome are very reminiscent of the features of algal
C
chloroplast genomes: For examSpheroid bodies
ple, it exists in the cell in two different forms that are caused by
rearrangements of the chromosome bracketed by inverted sequence repeat regions. Perhaps
UCYN-A and similar microorganisms (4, 9) effectively serve as
10 µm
10 µm
such nitrogen-fixing organelles.
Examples of unicellular symbioses. (A) Marine diatom with
The nature of single-celled
heterocyst-forming filamentous cyanobacterium. (B) Fluorescent
symbiosis is important for unin situ hybridization micrograph of UCYN-A (red) and its symbiotic
derstanding how organelles
partner, the prymnesiophyte Braarudosphaera bigelowii (green). Blue,
evolved and what the minimum
DAPI (4´,6-diamidino-2-phenylindole)-stained nucleus. Two types of
constraints for symbiosis are.
this cyanobacterium are now known: UCYN-A1 (left) and UCYN-A2
Symbiotic interactions with mul(right). (C) Rhopaloid freshwater diatom showing spheroid body.
ticellular plants or animals have
additional needs beyond the
example is a similar symbiosis between a
metabolic exchanges that form the core of
freshwater diatom and a nitrogen-fixing cynutritional, or syntrophic, mutualistic inanobacterium (simply called spheroid bodteractions. Signaling, mobility, cell and tisies; see the figure, panel C) with a small and
sue development, entrance through tissue
metabolically streamlined genome (9, 10).
or cell walls, tissue modifications, or strucBoth of these cyanobacterial genomes are
ture development are likely all unnecessary
greatly reduced compared to those of other
for a symbiosis that involves just two cells,
cyanobacteria. Although UCYN-A retains a
or a small number of cells. By contrast,
complete photosystem I, it does not evolve
transmission of the symbiotic partner to fuoxygen and may instead allow for energy or
ture generations of host cells may be critical
reductant production. The spheroid bodin the dilute ocean environment where conies have completely lost both photosystem
centrations of cells are low, and growth and
I and photosystem II. Both genomes have
cell division must be highly coordinated to
also lost part or all of the TCA (tricarboxylic
ensure that the growth of one partner does
acid) cycle, and have lost the ability to fix
not outstrip that of the other.
carbon dioxide into organic matter. They
In single-celled symbioses, both partners’
thus lack the defining characteristics of
growth and cell division must be coordicyanobacteria and are only cyanobacteria
nated. The UCYN-A prymnesiophyte host
1164
was first visualized with a single cyanobacterial cell (6). A few observations have now
been made of two UCYN-A cells on one
host (12), suggesting that the cyanobacterial
growth and division occur prior to the prymnesiophyte cell division. UCYN-A’s close relative UCYN-A2 (13) forms a cluster of a few
cells encased in a cellular pocket of the host
prymnesiophyte. It is unclear how this group
of cells grows and divides in synchrony with
the attached host prymnesiophyte cell.
It is not certain whether the UCYN-A
cyanobacteria are enclosed in a membrane.
One observation of UCYN-A (UCYN-A2)
suggests that the symbionts are intracellular (14). Regardless of its position inside or
outside the cell, there must be channels or
porters that allow exchange of fixed nitrogen for carbon, and perhaps even proteins,
as in the photosynthetic organelle of Paulinella (3). There are now many international
reports of UCYN-A, showing that the symbiosis is present at much wider geographic
scales than is typical for the better-known
oceanic nitrogen-fixing microorganisms
(12, 15). Many similar symbioses probably
exist in the environment, but are difficult to
detect or study because they are small, not
easily visualized or characterized, and difficult to manipulate experimentally. UCYN-A
and the freshwater diatom symbionts offer
a snapshot of what is likely to be found and
provide motivation for looking harder in
the environment for examples of microbial
symbiosis and, perhaps, organellar evolution in action. ■
REF ERENCES AND NOTES
1. E. T. Kiers, S. A. West, Science 348, 392 (2015).
2. D. K. Stoecker, M. D. Johnson, C. deVargas, F. Not, Aquat.
Microb. Ecol. 57, 279 (2009).
3. E. C. M. Nowack, A. R. Grossman, Proc. Natl. Acad. Sci.
U.S.A. 109, 5340 (2012).
4. T. A. Villareal, Mar. Ecol. Prog. Ser. 11, 117 (1990).
5. T. A. Villareal, Br. Phycol. J. 24, 357 (1989).
6. A. W. Thompson et al., Science 337, 1546 (2012).
7. J. P. Zehr, M. T. Mellon, S. Zani, Appl. Environ. Microbiol. 64,
3444 (1998).
8. H. J. Tripp et al., Nature 464, 90 (2010).
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(2014).
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8, 30 (2008).
11. J. Wouters, J. A. Raven, S. Minnhagen, S. Janson, Symbiosis
49, 61 (2009).
12. A. M. Cabello et al., ISME J. 10.1038/ismej.2015.147 (2015).
13. D. Bombar, P. Heller, P. Sanchez-Baracaldo, B. J. Carter, J. P.
Zehr, ISME J. 8, 2530 (2014).
14. K. Hagino, R. Onuma, M. Kawachi, T. Horiguchi, PLOS ONE
8, e81749 (2013).
15. M. Bentzon-Tilia et al., ISME J. 9, 273 (2015).
ACKNOWL EDGMENTS
This work was partially supported by the NSF Center for
Microbial Oceanography: Research and Education; a
Gordon and Betty Moore Foundation grant; and the Simons
Collaboration on Ocean Processes and Ecology (SCOPE).
Micrographs were provided by T. A. Villareal, R. Lowe, U. Maier
and S. Zauner, and M. del Carmen Muñoz-Marin.
10.1126/science.aac9752
sciencemag.org SCIENCE
11 SEP TEMBER 2015 • VOL 349 ISSUE 6253
Published by AAAS
PHOTOS: PANEL A, T. A. VILLAREAL; PANEL B, (LEFT) R. LOWE, (RIGHT) S. ZAUNER AND U. MAIER; PANEL C, M. DEL CARMEN MUÑOZ-MARIN
INSIGHTS | P E R S P E C T I V E S
How single cells work together
Jonathan P. Zehr
Science 349, 1163 (2015);
DOI: 10.1126/science.aac9752
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