Are low temperature habitats hot

spots of microbial evolution driven by

viruses?
Alexandre M. Anesio and Christopher M. Bellas
Bristol Glaciology Centre, School of Geographical Sciences, University of Bristol, Bristol BS8 1SS, UK
There is an increasing body of evidence to show that
viruses are important drivers of microbial evolution and
that they can store a great deal of the Earths microbial
diversity in their genomes. Examination of microbial
diversity in polar regions has revealed a higher than
expected diversity of viruses, bacteria and eukaryotic
microbes. Further, the few available studies in polar
regions reveal that viral control of microbial mortality
is important in these habitats. In this opinion article, we
argue that strong relationships between viruses and
their hosts in a range of polar habitats could be key in
explaining why polar regions are in fact hot spots of
microbial diversity and evolution. Further, we argue that
periodic glaciations, and particularly the Neoproterozoic
low-latitude glaciation, knownas snowball Earth, could
have been periods of intense diversication in aquatic
refuges.
Viruses as drivers of high microbial diversity
Viruses are the most abundant biological entity on the
planet [1]. They have been found in every biosphere inves-
tigated, and play a major role in aquatic ecosystems
through the destruction of their microbial hosts and sub-
sequent release of nutrients and carbon back in the dis-
solved pool. This short circuit of the microbial loop, known
as the viral shunt, is an important contributor to aquatic
carbon and nutrient cycling [2]. However, it is now becom-
ing clear that the viral inuence on natural habitats goes
much further than biogeochemical implications. Viruses
are potentially responsible for a great deal of microbial
diversity through interactions from the individual to the
community level, making the relationship between viruses
and hosts much more interwoven than previously thought.
At the community level, viruses can modify the micro-
bial community composition by the selective infection of
certain microbial hosts. The kill the winner hypothesis
was mathematically demonstrated by Thingstad and Lig-
nell [3], who proposed that when a population of bacteria
becomes dominant in aquatic systems as a result of a
combination of certain favourable conditions, the increase
in abundance enhances the chances for a bacterium within
a population to encounter an infectious virus (particularly
if we consider that viral infection is species- or genus-
specic and density-dependent). When a crucial threshold
of available hosts is reached, the host population becomes
infected and is destroyed. Whether the infected host strain
is replaced by a virus-resistant, closely related strain, or by
a different species, is unknown [4]. A mutation for virus
resistance is expected to come at a physiological cost to the
host, potentially allowing it to be outcompeted by other
bacteria with alternate virus binding sites [5]. However,
viral infection has also been shown to provide the selection
pressure necessary to maintain otherwise costly genes
within a population [6]. Marine bacterial communities
have been experimentally shown to differ when grown
with and without viruses [4], consistent with kill the
winner dynamics. Recently, this model has been further
developed [7], with the proposal of the constant diversity
dynamic model, in which phage predation pressure pre-
serves the diversity of niche-specialized prokaryotic popu-
lations. The kill the winner model is not just limited to
bacteriophages, as the same principles can be applied to
aquatic algae and their viral pathogens [8]. For example, in
mesocosm experiments and marine observations, the col-
lapse of blooms of the globally important marine alga
Emiliania huxleyi has been well documented, and attrib-
uted to viral lysis [9,10].
At the species level, virushost evolution is to some
extent driven by Red Queen interactions, with both virus
and host locked in a continual arms race. New strains of
viruses are continually selected for increased virulence to
Opinion
Glossary
Burst size: the number of viruses that are released from each initially infected
cell.
Lysogeny: a phage life strategy in which phage DNA becomes integrated with
that of its host. The phage is effectively dormant, and its genome is copied
alongside its host during replication until an environmental trigger causes the
virus to revert to the lytic cycle. Phages that can undergo lysogeny are known
as temperate phages.
Lytic cycle: one of the cycles of viral replication by which a virus enters a cell
and instructs its hosts cellular machinery to synthesize more virus particles.
The cell eventually bursts, releasing new infectious viruses.
Oligotrophic: a habitat characterized by low nutrients and productivity.
Pseudolysogeny: a phage carrier state in which the phage nucleic acid enters a
cell and remains dormant, establishing neither a lysogenic nor lytic infection.
Phages are not evenly transmitted to daughter cells.
Snowball Earth: a hypothesis that the Earth was entirely covered in ice during
the Proterozoic period.
Slushball Earth: an alternative hypothesis to the snowball Earth model, which
argues that open water and a thin covering of ice would have been found in
equatorial regions of snowball Earth.
Transduction: the process of transferring genetic material from one host cell to
another by incorporation into a virus genome.
Virome: the complete genomes of all viruses inhabiting a particular environ-
ment.
Corresponding author: Anesio, A.M. (a.m.anesio@bristol.ac.uk).
52 0966-842X/$ see front matter 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tim.2010.11.002 Trends in Microbiology, February 2011, Vol. 19, No. 2
create more infections, while hosts are selected for in-
creased resistance to viruses, leading to a relative balance
between the two [11]. Recently this has been conrmed at
the genomic level, where co-evolving viruses and hosts
produce phage populations with a greater genetic diversity
than do populations of phage and a non-evolving host [12].
The mixing of these antagonistically coevolving phage
host populations with others also further accelerates di-
versity at the phenotypic level of both the host and phage
[13]. It is evident that even simple unperturbed virushost
systems are undergoing continual change at both the
genetic and phenotypic level.
Viruses as mobile genetic reservoirs
Both lytic and temperate phages (lysogenic) are known to
transfer genetic material between hosts through transduc-
tion (see Glossary), a process by which host genes are
packaged up into a new virion and transferred to further
hosts during subsequent infection. Furthermore, during
lysogeny, newproperties might be conferred upon the hosts
through incorporation of viral genes. Well-known examples
include the transduction of virally encoded cholera toxin
genes (which cause enhanced virulence in Vibrio cholerae
bacteria) [14] and the virally mediated transfer of antibiotic
resistance genes between bacterial strains [15]. The scale of
this genetic transfer and implications for host diversity are
now becoming apparent. In the marine environment, it has
been estimated that transductions occur at a rate of 100
transductions per litre per day [16], or scaling up, 10
34
transductions of phage genes to hosts per year in the oceans
[17]. There is nowa growing body of evidence demonstrating
that many phagehost evolutionary histories have been
characterized by extensive gene transfer between virus
andhost [16,1820]. Anexample of this transfer inthe ocean
is thought to occur inProchlorococcus cyanophage genomes,
which regularly contain many genes acquired from their
cyanobacterial hosts, including genes for photosynthesis
[21]. Such genes are expressed during viral infection, and
are thought to allow photosynthesis and other essential
processes to continue for sufcient duration to allow pro-
duction of new virions when normal host protein synthesis
has been shut down [22].
Perhaps the most compelling evidence for viruses shap-
ing their hosts evolutionary history has come from recent
metagenomic studies. Comparing paired microbial and
virus metagenomic libraries for their functional potential
has revealed an extensive abundance of microbial meta-
bolic genes present in virus genomes [23], including genes
responsible for carbohydrate and protein metabolism, pho-
tosynthesis, and vitamin synthesis. Remarkably, viromes
corresponding to paired microbial metagenomes contain
all the functional diversity present in the microbial meta-
genome. It appears that viruses are a potential reservoir of
stored host genes [23] that can be transferred back and
forth and throughout the microbial population by trans-
duction. It has even been proposed that these stored genes
might provide the genetic adaptability to change the eco-
logical niche of their hosts [17]. When considering the
prospect that viruses are capable of moving between
biomes [24], the potential genetic reservoir that can inu-
ence a bacterial host is vast.
Virus activity in low temperature environments
Microbial diversity and activity in polar regions often
remains surprisingly high despite the constant low tem-
peratures. Even the apparently lifeless surface of glaciers
and the soils of the Dry Valleys of Antarctica have revealed
remarkable microbial diversity and activity [2529]. There
is particularly high microbial activity in aquatic habitats
that form in the ablation zones of glaciers, the so-called
cryoconite holes (Box 1). Cryoconite holes have recently
been considered as refuges for life in glacial systems, and
could have been an important pocket for active microbial
food webs and evolution during the snowball Earth (see
below and Box 2).
The importance of viruses in biogeochemical cycling has
been documented throughout polar regions, including pe-
rennially ice covered lakes [30] and cryoconite holes [31].
Viruses are found in abundance in many polar regions,
even locked within the ice itself [3133]. Viral abundances
in polar inland waters vary greatly, with values ranging
Box 1. Cryoconite holes as refuges for microbial life at the
surface of glaciers
Cryoconite holes are distributed in glaciers worldwide, can cover 1
10% of the glacial surface, and are colonized by a diverse range of
microorganisms, including viruses, prokaryotic and eukaryotic
organisms [26,31]. There is an increasing body of evidence to show
that microbial activity in the holes is high, and can strongly
influence the biogeochemistry of glacial habitats [25,28]. The
cryoconite holes in Antarctica have an ice lid because of the
extreme low air temperatures, but absorption of heat from the
sediment still promotes melting from within the hole [52]. Despite
their isolated nature (Figure I), entombed cryoconite holes also
harbour active microbial communities that certainly contribute to
the formation of organic matter within the system, with photo-
synthesis rates higher than respiration, as indicated by extremely
high pH and extremely low partial pressure of CO
2
(pCO
2
) values
found in these habitats [53].
(a)
Glacier surface
Organic and
inorganic debris
(b) (c)
TRENDS in Microbiology
Figure I. Cryoconite holes. (a) Schematic diagram of cryoconite hole
formation. Cryoconite holes at the surface of glaciers are formed because
organic and inorganic particles, which are darker than the surrounding white
icy surface, absorb the solar radiation better than the ice. The heated debris
therefore melts into the ice forming holes, which provide nutrients and liquid
water for microbial activity. (b) Example of open cryoconite holes in the Arctic.
(c) Example of entombed cryoconite hole in Antarctica. Photo courtesy Liz
Bagshaw.
Opinion Trends in Microbiology February 2011, Vol. 19, No. 2
53
from 2.0 10
7
virus-like particles (VLP) per liter to
1.0 10
11
VLP/l [34]. The lower viral abundances in this
range are found in ultraoligotrophic Antarctic lakes and
glacial ecosystems. Mean abundances of polar freshwaters
are lower than temperate freshwater systems, but their
effect on microbial mortality is still high [31]. Further,
some of the Antarctic saline lakes have virus abundances
that overlap and exceed temperate marine systems [31].
Rates of viral production for polar inland waters of
2.0 10
6
to 2.0 10
9
VLP/l/h [30,3436] have been deter-
mined, where the higher end of this range overlaps with
rates found in productive temperate aquatic systems [37].
Thus, the lowtemperatures of polar habitats do not impede
viral activity and their potential to infect microbial popu-
lations. In fact, bacterial communities in many polar habi-
tats, especially the Antarctic and glacial ecosystems
worldwide, have fewspecies of grazers [34], and thus, virus
infection can be responsible for a large percentage of
bacterial mortality, outcompeting grazing in many of these
systems [34,36,38]. The pressure exhibited by viruses is
likely to be the main controlling biological factor on these
microbial communities. The positive correlation between
virus and bacterial abundance in many polar aquatic
systems supports this view [34]. Hence, community modi-
cation by viruses could be a signicant driver of microbial
diversity, playing a greater role in these extreme cold
habitats.
Viral infections in some polar environments exhibit
unusual characteristics in that the frequency of visible
infected bacterial cells is much higher than in temperate
aquatic habitats, whereas burst sizes are unusually low
[39]. In polar ultraoligotrophic regions, viruses visibly
infect an average of 26% of the bacterial community
[39], which is an order of magnitude higher than in tem-
perate systems, and the actual level of infection is certainly
higher, as visible infection occurs only in the latter stages
of viral infection. To maintain these high infection rates in
an oligotrophic habitat with low microbial abundance (and
thus with lower chances for encounters between viruses
and their hosts), it is hypothesized that viruses in some of
these systems are more opportunistic in their infection
strategy, having a potentially broad host range [31], which
could maximize viral infections. The consequence of such a
large percentage of the microbial community being infected
by viruses is likely to be an increase in the selection
pressure exerted by viruses to stimulate a more diverse
bacterial community.
Lysogeny and pseudolysogeny in low temperature
habitats
Lysogeny has often been suggested to be a phage life
strategy used to cope with unfavourable conditions for
virus propagation via the lytic cycle [37,40] and thus, this
strategy could play a greater role in low temperature
habitats, particularly in ultraoligotrophic lakes and glacial
ecosystems. The few datasets available indicate that ly-
sogeny varies greatly in polar environments, with esti-
mates of up to 73% of bacteria harbouring lysogenic
viruses [34]. Interestingly, two seasonal studies of lysogeny
in the Antarctic found high incidence of lysogeny in the
Austral winter and spring and a complete absence in the
summer months [35,36], consistent with this hypothesis.
No lysogeny has been detected in Arctic freshwater envir-
onments during the summer [38]. The picture could be
unclear because many of the polar freshwaters studied are
ultraoligotrophic, and it is possible that these conditions
result in viruses establishing an alternative relationship
with their hosts, so-called pseudolysogeny. Pseudolyso-
geny is a phage carrier state outwardly similar to lysogeny,
but is in fact an arrested lytic cycle. The phage genome does
not integrate with that of its host, and crucially is not
inducible by current experimental methods [37]. It has
been hypothesized that during nutrient limitation, an
infected cell is unable to sustain phage replication until
nutrients are replenished [41], and that this process could
incapacitate viral assembly and allow the viral genome to
stay inside the host. Several laboratory and mesocosm
studies have shown that viruses establish a potential
pseudolysogenic relationship with their hosts in response
to nutrient limitation [4143]. In these studies, viral burst
sizes were signicantly reduced (up to 80%), and large
numbers of phage particles were only released when nutri-
ents were added back to the system. Scanlan and Wilson
[43] reported that lysis rates of infected cells decreased by a
factor of 10 in nutrient limited systems, leaving a large
fraction of the infected community intact. Such a pseudo-
lysogenic strategy in viruses is thought to allow viruses to
maintain themselves within a bacterial population despite
low host abundances and through unfavourable times [37].
The fact that a very high frequency of infected cells with
Box 2. Evolution and extinction of life during snowball
Earth
Snowball Earth is commonly defined as the period when the Earth
was nearly or completely covered by ice, between approximately
750 million and 580 million years ago in the Neoproterozoic Era.
Sedimentary deposits of glacial origin at tropical paleolatitudes are
a strong argument for the hypothesis that the Earths surface
became nearly or entirely frozen [54]. The environmental conditions
during the snowball Earth could have been represented by mean
annual temperatures well below freezing, and the oceans would
have been covered with ice [54]. There is still debate about the
interpretation of the sedimentological evidence that gave strength
to the snowball hypothesis [55].
Further, the implications for life on a frozen Earth would have led
the diversity of the microbiota to be substantially different
compared with the period just before snowball Earth. However,
such change in diversity and composition of the microbiota has
rarely been observed [49,50]. Advocates of the snowball hypothesis
argue that microbial diversity could have survived in refuges of life
such as brine channels, transient meltwater ponds, and subglacial
environments [56]. All of these potential extreme habitats currently
have corresponding modern versions, which are colonized by both
cosmopolitan and highly specialized microbial communities [57].
Nevertheless, although biological activity and diversity could have
been preserved in these refuges, the duration of the snowball Earth
period (millions of years) would have been too long, eventually
leading to the degeneration and collapse of microbial life in such
refuges. The later has led to a slushball Earth hypothesis, which
suggests that some sort of hydrologic cycle and interconnectivity
between refuges of life must have existed to provide channels for
dispersal of genes and nutrients [50]. Alternatively, the presence of
several refuges during a snowball Earth scenario could also provide
opportunities for evolution to occur by taking different directions
around the planet, which would have resulted in even higher
available diversity once the Earth had returned to a warmer state.
Opinion
Trends in Microbiology February 2011, Vol. 19, No. 2
54
unusual low burst sizes are observed in the ultraoligo-
trophic low temperature habitats of the Arctic and
Antarctica [39] suggests that such a pseudolysogenic rela-
tionship might be established until favourable conditions
are reached. In typical temperate aquatic systems, phages
are continually destroyed, and their average half-lives in
the environment are only a few days [44]. If conditions in
low temperature habitats are limiting for their hosts, and
host abundance is too low to support lytic interaction, a
lysogenic and/or pseudolysogenic relationship effectively
extends the life of a particular virus strain in the environ-
ment [41], potentially allowing a greater maintenance of
viral particles and existence of diversity in extreme con-
ditions. However, considering the scarcity of data available
on viral activity and ecology fromextreme lowtemperature
environments, those hypotheses are yet to be tested.
Recent metagenomic investigations on Antarctic viral
communities have uncovered the greatest virus diversity
recorded in a single aquatic viral metagenome [45]. As
virus diversity is high, it is likely that this diversity is
reected in the pool of host-derived genes, thus inuencing
host diversity through both community modication and
transduction. The Antarctic virome is the most diverse yet
discovered and the potential for transfer of host-acquired
genes is therefore greater than for many other non-cold
environments. However, the diversity of other Antarctic
and isolated Arctic freshwater viromes remains to be
explored. A study of marine viromes showed less viral
diversity in the Arctic Ocean than in temperate regions
[46], but we argue that the ideas presented here apply
particularly to isolated inland low temperature habitats.
The high frequency of infection and the potential lysogenic
and pseudolysogenic strategies in these isolated low
temperature habitats could favour more viralhost inter-
actions and could prolong the length of time that phage
genomes stay in the environment relative to temperate
regions. This, in combination with top-down control of
microbial communities that could be dominated by viruses
(as opposed to grazing), could explain why cold habitats are
in fact hot spots of microbial diversity and evolution
(Figure 1). Further, because of their transportability and
genetic exibility, viruses have a broad distribution in the
environment [47]. Genes from global populations might
ow into polar regions through viruses, and inuence
microbial diversity, while strong relationships between
viruses and their host in low temperature habitats could
help to preserve and even intensify the microbial evolution
of these habitats.
Implications for glaciation events and in other extreme
environments
Periodic glaciation, and particularly the Neoproterozoic
low-latitude glaciation known as snowball Earth, could
have been periods of intense diversication rather than
periods of major extinctions in microbial communities (Box
2). Old and diverse lineages of microbes typical of low
temperature habitats could have survived in cold refuges
(e.g. cryoconite holes) throughout the Earths history.
Stoeck et al. [48] found higher diversity of ancestral
lineages of microbial eukaryotes in cold habitats relative
to hot environments, consistent with selection for cold-
adapted genes during periods of glaciations. Evidence from
the microfossil record from the Death Valley region in
California even indicates a slightly more diverse micro-
biota development during the snowball Earth period [49].
The high viral infection rates observed in low temperature

Low temperature habitats Average temperature habitats
Infection rates,
burst sizes and
pseudolysogeny
Top-down controls
(grazing vs viral
infection)
V
B
VG BG
Lysogeny and
spectrum of
infection
= =
F
(a)
(b)
(c)
TRENDS in Microbiology
Figure 1. Conceptual model of interactions between viruses and bacteria in cold-oligotrophic conditions. These interactions could maintain and promote microbial diversity in
low temperature habitats. (a) High infection rates, (b) a virus-dominated top-down control of microbial populations, and (c) high incidence of lysogeny and broad spectrum of
infection could all promote high rates of transduction and genetic diversification. (a) Evidence from the literature indicates that the number of visibly infected bacteria in
ultraoligotrophic lakes in Antarctica and cryoconite holes in the Arctic are one order of magnitude higher than those fromtemperate aquatic habitats. The low burst sizes in low
temperature habitats could also indicate a pseudolysogenic relationship between viruses and their hosts. (b) For top-down controls, bacterial mortality in temperate aquatic
habitats is on average equally controlled by viruses and protozoan grazing, although we conceptualize that virus infection is the major control in more extreme habitats, as a
result of the truncated nature of their microbial food webs. (c) The outcome of a virus and host encounter in low temperature habitats is hypothesized to result in more
opportunities for transduction as a result of high infection rates, lysogenic strategies and broad spectrumof infection relative to encounters between viruses and potential hosts
in warmer and nutrient richer habitats. Abbreviations: B, bacteria; BG, bacterial genome; F, heterotrophic nanoflagelates; V, virus; VG, viral genome.
Opinion Trends in Microbiology February 2011, Vol. 19, No. 2
55
habitats could have stimulated microbial diversication
and evolution, with important consequences for the bio-
sphere during cold climatic conditions. The list of evidence
in the literature of unicellular eukaryotic and prokaryotic
organisms that survived the snowball Earth period keeps
growing [50]. The evidence that microbial diversity was
kept unchanged during the snowball Earth period led
Moczydowska [50] to suggest that a slushball Earth
model, with an open hydrological cycle, would be more
adequate to explain the high microbial diversity that
survived the Cryogenean period. We suggest that the
nature of the microbial food webs during the Cryogenean
period, potentially dominated by viral infections as con-
trols of microbial mortality, could also have helped the
preservation of diversity, and even stimulated diversica-
tion and evolution within the microbial community. We do
not imply that a snowball Earth model is better than the
slushball Earth model, which is beyond the scope of this
article. However, we believe that preservation of genes and
evolution driven by viruses could have occurred in aquatic
refuges even without a functional and open hydrological
cycle. If microbes from warmer regions became extinct
during glaciations, the genetic reservoir in viruses in the
cryosphere could resupply some of the temperate host
genes when the ice receded.
Concluding remarks
New evidence from laboratory experiments, modelling
exercises and eld data shows that viruses are important
drivers of microbial evolution. In this article, we argue that
polar regions are potential hot spots of microbial diversity
and evolution, because of the strong relationships between
viruses and their hosts in these habitats. The few data
available frompolar regions reveal that viral activity is not
limited by low temperatures, and that other strategies,
such as a broad host range, lysogeny and pseudolysogeny,
might create even more opportunities for interactions
between viruses and their hosts. The same mechanism
for preservation of microbial diversity proposed here for
extreme low temperature habitats could also explain the
unexpectedly high microbial diversity found in other ex-
treme habitats, where microbial food webs are potentially
dominated by viral control. An example is the deep-sea
benthos, where recent studies have shown that viruses
have the ultimate top-down control of microbial food webs,
being responsible for almost all the heterotrophic microbial
mortality [51]. Cold habitats are substantially well repre-
sented on Earth. Tapping into the virome of these extreme
habitats could reveal a range of genes carrying vital bio-
geochemical functions that have shaped modern global
biogeochemical cycles on our planet.
Many of the opinions discussed above are speculative
because the availability of data on viral diversity and
activity in low temperature habitats is still very limited.
More surveys of viral diversity in low temperature habi-
tats, particularly in relatively isolated systems, are neces-
sary to demonstrate that microbial diversity in those
systems is unexpectedly high and that virus genomes
might contain important microbial metabolic genes, in-
cluding those responsible for adaptation of life to cold
conditions (Box 3). The high viral activity in cold conditions
could have helped to preserve and even might have stimu-
lated microbial diversity during periodic glaciations, and
particularly the Neoproterozoic low-latitude glaciation,
known as snowball Earth.
Acknowledgements
This research is funded by the UK Natural Environmental Research
Council (NERC - NE/G00496X/1) to AMA. CMB is funded by a NERC
Doctoral Training Programme grant. We would thank Professor
Laybourn-Parry, Dr. Gail Teitzel and two anonymous referees for
constructive comments on earlier versions of this manuscript.
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