HydrogenHypothesis

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Current Biology
Dispatches
researchers a molecular foothold into
mechanisms underlying the activation
of the hygroreceptor as well as the
encoding of humidity in the brain.
Additional work will be necessary to
determine whether hygrosensory
neurons outside the sacculus [8,15],
like the ones expressing waterwitch
or nanchung, represent a parallel
class of hygrosensory neurons that
supplement saccular responses.
Molecular identification of all three
receptors in the hygrosensory triad will
permit the exploration of biophysical
principles underlying activation of the
hygroreceptor. This will also generate
tools to explore other compelling
questions such as how humidity
and temperature information interact
in the brain and how the relevant
neural circuits determine humidity
set-points in different Drosophila
species.
REFERENCES
1. Tichy, H. (1987). Hygroreceptor identification
and response characteristics in the stick
insect Carausius morosus. J. Comp. Physiol. A
160, 43–53.
2. Altner, H., and Loftus, R. (1985). Ultrastructure
and function of insect thermo- And
hygroreceptors. Annu. Rev. Entomol. 30,
273–295.
3. Yokohari, F. (1978). Hygroreceptor
mechanism in the antenna of the cockroach
Periplaneta. J. Comp. Physiol. A 124, 53–60.
4. Enjin, A., Zaharieva, E.E., Frank, D.D.,
Mansourian, S., Suh, G.S.B., Gallio, M., and
Stensmyr, M.C. (2016). Humidity sensing in
Drosophila. Curr. Biol. 26, 1352–1358.
5. Bentley, I.M. (1900). The synthetic experiment.
Am. J. Psychol. 11, 405.
6. Filingeri, D., and Havenith, G. (2015). Human
skin wetness perception: psychophysical and
neurophysiological bases. Temperature 2,
86–104.
7. Russell, J., Vidal-Gadea, A.G., Makay, A.,
Lanam, C., and Pierce-Shimomura, J.T.
(2014). Humidity sensation requires both
mechanosensory and thermosensory
pathways in Caenorhabditis elegans.
Proc. Natl. Acad. Sci. USA 111, 8269–8274.
8. Liu, L., Li, Y., Wang, R., Yin, C., Dong, Q., Hing,
H., et al. (2007). Drosophila hygrosensation
requires the TRP channels water witch and
nanchung. Nature 450, 294–298.
9. Sayeed, O., and Benzer, S. (1996). Behavioral
genetics of thermosensation and
hygrosensation in Drosophila. Proc. Natl.
Acad. Sci. USA 93, 6079–6084.
10. Abuin, L., Bargeton, B., Ulbrich, M.H.,
Isacoff, E.Y., Kellenberger, S., and Benton,
R. (2011). Functional architecture of olfactory
ionotropic glutamate receptors. Neuron 69,
44–60.
11. Larsson, M.C., Domingos, A.I., Jones, W.D.,
Chiappe, M.E., Amrein, H., and Vosshall,
L.B. (2004). Or83b encodes a broadly
expressed odorant receptor essential
for Drosophila olfaction. Neuron 43,
703–714.
12. Shanbhag, S.R., Singh, K., and Singh, R.N.
(1995). Fine structure and primary sensory
projections of sensilla located in the
sacculus of the antenna of Drosophila
melanogaster. Cell Tissue Res. 282,
237–249.
13. Silbering, A.F., Rytz, R., Grosjean, Y., Abuin,
L., Ramdya, P., Jefferis, G.S.X.E., et al. (2011).
Complementary function and integrated wiring
of the evolutionarily distinct Drosophila
olfactory subsystems. J. Neurosci. 31,
13357–13375.
14. Su, C.-Y., Menuz, K., Reisert, J., and Carlson,
J.R. (2012). Non-synaptic inhibition between
grouped neurons in an olfactory circuit. Nature
492, 66–71.
15. Yao, C.A., Ignell, R., and Carlson, J.R. (2005).
Chemosensory coding by neurons in the
coeloconic sensilla of the Drosophila antenna.
J. Neurosci. 25, 8359–8367.
Mitochondrial Evolution: Going, Going, Gone
Fabien Burki
Science for Life Laboratory, Program in Systematic Biology, Department of Organismal Biology, Uppsala University, Norbyvägen 18D,
75236 Uppsala, Sweden
Correspondence: [email protected]
http://dx.doi.org/10.1016/j.cub.2016.04.032
Monocercomonoides is the first example of a eukaryote lacking even the most reduced form of a
mitochondrion-related organelle. This has important implications for cellular processes and our
understanding of reductive mitochondrial evolution across the eukaryotic tree of life.
The origin of mitochondria by the
endosymbiotic integration of an
a-proteobacterium is one of the defining
events in eukaryote evolution. Although
the details of this endosymbiosis are
still unclear [1,2], more than two decades
of molecular evolution and cell biology
research have demonstrated that the
origin of mitochondria predated the
divergence of all known eukaryotes.
This means that all extant eukaryotes,
or at least their ancestral lineages, are
predicted to harbor mitochondria in
one way or another. And indeed, all
species studied to date have been
found with either canonical aerobic
mitochondria, or less conventional
but evolutionarily linked mitochondrionrelated organelles (MROs) in anaerobic
and microaerophilic lineages (Figure 1).
MROs are loosely defined as degenerated
mitochondria exhibiting various degrees
R410 Current Biology 26, R408–R431, May 23, 2016
of reduction. They represent a continuum
from anaerobic mitochondria (generate
ATP using alternative electron acceptors),
to more reduced hydrogenosomes
(generate ATP via substrate-level
phosphorylation, lack an electron
transport chain, produce hydrogen),
to highly reduced mitosomes (no role
in ATP production, lack an electron
transport chain, involved in iron-sulfur
cluster assembly) [3,4]. So all extant
Current Biology
Dispatches
eukaryotes possess organelles related
to mitochondria, right? Not anymore,
as we are told by Karnkowska and
colleagues in this issue of Current
Biology [5], reporting on the recent
genome sequencing of the anaerobic
microbe Monocercomonoides sp.
Demonstrating absence is a daunting
task. To provide a compelling case for
the complete lack of mitochondrial
organelles in Monocercomonoides sp.,
Karnkowska et al. set out on a range of
bioinformatic experiments. First, they
show that their draft genome is virtually
complete. With that in hand, they confirm
that no mitochondrial genome is to be
found, which comes as little surprise, as
many MROs lost their genome long ago,
and mitochondrial metabolism in
general is sustained by proteins encoded
in the nucleus [6]. Some of these
nucleus-encoded proteins represent
hallmarks of mitochondrial function,
and are typically associated with MROs
in other organisms. These include the
homologous core of the protein import
machinery, transporters of the
mitochondrial carrier family, or the
mitochondrial iron-sulfur (Fe-S) cluster
assembly [7]. Not in Monocercomonoides
sp., which lacks all of them. To be
comprehensive, the authors also
looked at a larger database of known
mitochondrial proteins, and expanded
their hunt beyond homology searches to
look for signature sequence motifs
such as mitochondrial targeting
signals. Needless to say, none of these
approaches came back positive,
allowing Karnkowska et al. to infer the
general absence of mitochondrial
proteins in Monocercomonoides sp.,
and by extension the unprecedented
report of a eukaryote without any kinds
of mitochondrial organelles.
Of course, not having a mitochondrial
organelle at all has biological
implications that the organism must
cope with. In the first place, how
does Monocercomonoides sp. generate
its energy? As stated above, MROs
towards the most reduced end of
the spectrum (e.g. mitosomes) have
already lost the ability to produce ATP.
Organisms with such organelles use
other means instead, for example
importing ATP from host cells in the
case of intracellular parasites [8], or
completely outsourcing the production
‘Textbook’
Mitochondrion
Anaerobic
Mitochondrion
Hydrogenosome
Mitosome
ee-
Loss of MRO in
Monocercomonoides
ee-
O2
Not O2
ATP
ISC
ISC
ATP
ISC
ISC
ATP
H2
Mitochondrial
genome
Generate ATP but oxygen is
not the ternimal electron
Oxidative phosphorylation to
acceptor; other compounds
generate ATP; oxygen is the
are used, such as fumarate.
terminal electron acceptor.
Most reduced MRO; no No more
detectable MRO
electron transport; no
oxidative phosphorylaNo oxidative phosphoryla- tion; no ATP generation;
participate in Fe-S cluster
tion, ATP is generated
instead by substrate-level biosynthesis, localization
phosphorylation; produce of the ISC pathway.
hydrogen.
Current Biology
Figure 1. Mitochondrial reductive evolution.
Very simplified view of mitochondria and related organelles. Major distinguishing features are shown
(e.g., presence of a genome, electron transport chain, ATP production, ISC pathway), but by no means
represent the full set of metabolic pathways (except for mitosome). Only discrete categories are shown,
which do not represent the reality as many intermediate organelles have been described. The ISC
pathway is the only function that exists throughout mitochondria and MRO diversity.
of ATP to the cytoplasm by substratelevel phosphorylation in glycolytic
reactions [3]. Monocercomonoides sp.
apparently does just that, as deduced
by the presence of a full glycolysis
pathway as well as anaerobic
fermentation enzymes [5].
Another implication of missing an
MRO, in many ways more puzzling, is
the absence of a mitochondrial Fe-S
biosynthesis pathway (ISC). Fe-S
clusters are cofactors of proteins that
play essential roles in many cellular
reactions, such as electron transport or
enzyme catalysis. To be assembled
properly in eukaryotes, Fe-S clusters
require the joint action of the ISC pathway
and its cytosolic counterpart, the CIA
pathway [9]. This places the ISC
pathway in a pivotal position for the
proper functioning of cellular processes,
and indeed has been regarded as the
only unifying feature of mitochondria
and MROs (Figure 1) [10]. So how does
Monocercomonoides sp. assemble
Fe-S clusters without an MRO? The
answer, quite literally, comes from
bacteria. Instead of the ISC pathway,
Monocercomonoides sp. possesses
bacterial genes encoding components
of the sulfur mobilization (SUF) machinery,
one of the prokaryotic systems that can
assemble Fe-S clusters [11]. Acquired
through lateral gene transfers (LGTs)
from bacteria, these genes seemingly
replaced the ISC system in
Monocercomonoides sp., allowing it to
fulfill the Fe-S biosynthesis requirements
right from the cytosol. The precise timing
of the SUF acquisition is unknown, but
Karnkowska et al. propose that both
the SUF and ISC systems have
coexisted during some time [5]. This is
a reasonable assumption because a
relative species, Paratrimastix pyriformis,
was found to have homologs of the
same SUF system, most likely acquired
in a common ancestor, although it
remains to be seen whether P. pyriformis
has also retained the ISC pathway.
The hypothesized co-occurrence of
the SUF and ISC systems in an ancestral
lineage of Monocercomonoides sp.
brings us to the heart of the issue. By
creating redundancy, it is now possible
to explain how Monocercomonoides sp.
became completely amitochondriate.
Specifically, the ISC pathway was no
longer required since the SUF pathway
can perform similar functions, making it
dispensable and ultimately resulting in
the complete loss of mitochondria. If
correct, this scenario would reinforce
our understanding of the minimal
function of mitochondria, that is, in Fe-S
cluster biosynthesis [10]. However,
evolution generates diversity in infinite
ways, and the mosaic of functions found
in MROs is a prime example of that.
Although still extremely rare, two other
Current Biology 26, R408–R431, May 23, 2016 R411
Current Biology
Dispatches
cases of replacement of the ISC system
are known in unrelated microbial
lineages. These are Archamoebae and
the breviate amoeba Pygsuia biforma,
which have instead a bacterial nitrogenfixation (NIF) system and an archaeal
SUF machinery, respectively [12,13]. In
both cases, Fe-S requiring enzymes
(e.g. [FeFe]-hydrogenase) have been
retained along with the MROs where
they function, in spite of the absence
of the ISC system. Clearly, the situation
is different in Monocercomonoides sp.,
which streamlined its mitochondrial
function to the extreme — the loss of
the organelle. So in such a complex
array of organelles and functions,
pinpointing an exact set of causes for
mitochondrial loss is premature. It is
likely that reductive mitochondrial
evolution in Monocercomonoides sp.
and MRO-containing lineages is not just
the result of genetic opportunities (e.g.
LGTs) and functional redundancy. Other
forces are at play, including chance,
biological constraints due to specific
lifestyles (e.g. energy requirement), as
well as varying responses to
environmental conditions.
More generally, such comparisons
across the eukaryotic diversity vividly
remind us, if need be, of the importance
of discovery science. Our current
understanding of eukaryote diversity
and evolution (see [14] for a recent
review) compels us to interpret the
absence of mitochondrial organelles in
Monocercomonoides sp. as a derived
state. It would have been different 20
years ago, under the so-called Archezoa
hypothesis, which postulated that some
microbial eukaryote lineages diverged
before the mitochondrial endosymbiosis,
thus ancestrally lacking mitochondria
[15]. If today we are confident in the
secondarily amitochondriate nature of
Monocercomonoides sp., it is because of
the continuing discovery and functional
characterization of a wide range of
MROs in diverse lineages, as well as the
improved resolution of the eukaryotic
tree. The vast majority of eukaryotic
diversity is composed of unicellular
microbes — the protists — that, much
like Monocercomonoides sp., are key to
understanding the evolutionary paths
that gave rise to this biodiversity. As
shown here by Karnkowska and
co-authors [5], genome sequencing is
a powerful tool that can shed light on
extraordinary cellular and evolutionary
processes in unexplored parts of the
biosphere. Current research has
barely scratched the surface of
protist diversity; it is now time to dig
deeper.
7. Shiflett, A.M., and Johnson, P.J. (2010).
Mitochondrion-related organelles in
eukaryotic protists. Annu. Rev. Microbiol. 64,
409–429.
REFERENCES
9. Stehling, O., and Lill, R. (2013). The role of
mitochondria in cellular iron-sulfur protein
biogenesis: mechanisms, connected
processes, and diseases. Cold Spring
Harb. Perspect. Biol. 5, a011312–2.
1. Poole, A.M., and Gribaldo, S. (2014).
Eukaryotic origins: how and when was the
mitochondrion acquired? Cold Spring Harb.
Perspect. Biol. 6, a015990.
2. Pittis, A.A., and Gabaldón, T. (2016). Late
acquisition of mitochondria by a host with
chimaeric prokaryotic ancestry. Nature 531,
101–104.
3. Müller, M., Mentel, M., van Hellemond, J.J.,
Henze, K., Woehle, C., Gould, S.B., Yu, R.Y.,
van der Giezen, M., Tielens, A.G., and Martin,
W.F. (2012). Biochemistry and evolution of
anaerobic energy metabolism in eukaryotes.
Microbiol. Mol. Biol. Rev. 76, 444–495.
4. Stairs, C.W., Leger, M.M., and Roger, A.J.
(2015). Diversity and origins of anaerobic
metabolism in mitochondria and related
organelles. Phil. Trans. R. Soc. B 370,
20140326.
5. Karnkowska, A., Vacek, V., Zubacova, Z.,
Treitli, S., Petrzelkova, R., Eme, L., Novák, L.,
Zárský,
V., Barlow, L.D., Herman, E.K., et al.
(2016). A eukaryote without a mitochondrial
organelle. Curr. Biol. 26, 1274–1284.
6. Timmis, J.N., Ayliffe, M.A., Huang, C.Y., and
Martin, W.F. (2004). Endosymbiotic gene
transfer: organelle genomes forge
eukaryotic chromosomes. Nat. Rev. Genet.
5, 123–135.
8. Tsaousis, A.D., Kunji, E.R.S., Goldberg, A.V.,
Lucocq, J.M., Hirt, R.P., and Embley, T.M.
(2008). A novel route for ATP acquisition by
the remnant mitochondria of Encephalitozoon
cuniculi. Nature 453, 553–556.
10. Lill, R. (2009). Function and biogenesis of ironsulphur proteins. Nature 460, 831–838.
11. Takahashi, Y., and Tokumoto, U. (2002).
A third bacterial system for the assembly of
iron-sulfur clusters with homologs in archaea
and plastids. J. Biol. Chem. 277, 28380–
28383.
12. van der Giezen, M., Cox, S., and Tovar, J.
(2004). The iron-sulfur cluster assembly genes
iscS and iscU of Entamoeba histolytica were
acquired by horizontal gene transfer. BMC
Evol. Biol. 4, 7.
13. Stairs, C.W., Eme, L., Brown, M.W., Mutsaers,
C., Susko, E., Dellaire, G., Soanes, D.M.,
van der Giezen, M., and Roger, A.J. (2014).
A SUF Fe-S cluster biogenesis system in
the mitochondrion-related organelles of the
anaerobic protist Pygsuia. Curr. Biol. 24, 1176–
1186.
14. Burki, F. (2014). The eukaryotic tree of life
from a global phylogenomic perspective.
Cold Spring Harb. Perspect. Biol. 6,
a016147–7.
15. Cavalier-Smith, T. (1987). Eukaryotes with no
mitochondria. Nature 326, 332–333.
Imitation: Not in Our Genes
Cecilia Heyes
All Souls College and Department of Experimental Psychology, University of Oxford, Oxford
OX1 4AL, UK
Correspondence: [email protected]
http://dx.doi.org/10.1016/j.cub.2016.03.060
A powerful longitudinal study has failed to find any evidence that
newborn babies can imitate facial gestures, hand movements or
vocalisations. After 40 years of uncertainty, these findings indicate
that humans learn to imitate; this capacity is not inborn.
Humans are hyper-social animals. We
depend on cooperation with others —
relatives, friends, and strangers — to
fulfil our basic needs, and to learn the
R412 Current Biology 26, R408–R431, May 23, 2016
knowledge and skills that make human
lives so very different from those of
other animals. Since the 1970s [1],
many scientists have been convinced
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