Integrative and Comparative Biology
Integrative and Comparative Biology, volume 56, number 4, pp. 493–499
doi:10.1093/icb/icw094
Society for Integrative and Comparative Biology
SYMPOSIUM
Life on the Edge—the Biology of Organisms Inhabiting Extreme
Environments: An Introduction to the Symposium
Annie R. Lindgren,1 Bradley A. Buckley, Sarah M. Eppley, Anna-Louise Reysenbach,
Kenneth M. Stedman and Josiah T. Wagner
The Center for Life in Extreme Environments, Portland State University, Portland, OR 97201, USA
From the symposium ‘‘Life on the Edge: the Biology of Organisms Inhabiting Extreme Environments’’ presented at the
annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2016 at Portland, Oregon.
1
E-mail: [email protected]
Synopsis Life persists, even under extremely harsh conditions. While the existence of extremophiles is well known, the
mechanisms by which these organisms evolve, perform basic metabolic functions, reproduce, and survive under extreme
physical stress are often entirely unknown. Recent technological advances in terms of both sampling and studying
extremophiles have yielded new insight into their evolution, physiology and behavior, from microbes and viruses to
plants to eukaryotes. The goal of the ‘‘Life on the Edge—the Biology of Organisms Inhabiting Extreme Environments’’
symposium was to unite researchers from taxonomically and methodologically diverse backgrounds to highlight new
advances in extremophile biology. Common themes and new insight that emerged from the symposium included the
important role of symbiotic associations, the continued challenges associated with sampling and studying extremophiles
and the important role these organisms play in terms of studying climate change. As we continue to explore our planet,
especially in difficult to reach areas from the poles to the deep sea, we expect to continue to discover new and extreme
circumstances under which life can persist.
Introduction
As humans, our bounds of a habitable environment
encompass only a fraction of the available space on
Earth. Research in the last several decades has expanded understanding of how persistent life truly
is—from Antarctic fish that survive in waters constantly near or below 08C and sea anemones that
burrow within the ice—to hydrothermal vent microbes that thrive in a high pressure, high temperature environment, and live off of noxious
compounds such as sulfide and methane—to large,
muscular squids living in oxygen minimum zones.
As our climate continues to change, it is these extremophiles that could provide us with insight into
the future: perhaps by uncovering the molecular and
biochemical tools these extremophiles employ, we
will better understand how life in general will
respond.
How do we delineate ‘‘extreme’’ from ‘‘normal’’
habitats? From an organismal perspective, extreme is
relative: microbes living at high temperatures near
hydrothermal vents would consider our ‘‘normal’’
freezing. For the purposes of this symposium, we
take a generalist standpoint: an extreme environment
is one in which some physical or biological factor
falls at the very edge of a normal range, making it
uninhabitable to humans or many typical model organisms such as Escherichia coli or Caenorhabditis
elegans (Morita 1999; Rothschild and Mancinelli
2001). Extreme habitats are largely defined not only
by extreme highs and lows in abiotic/physical characteristics including temperature, pressure, pH,
oxygen saturation, salinity, but can also be influenced by biological characteristics such as low nutrition, high population density, or low prey availability
(Rothschild and Mancinelli 2001). Some of the most
‘‘extreme’’ environments on Earth include hot
Advanced Access publication July 28, 2016
ß The Author 2016. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.
All rights reserved. For permissions please email: [email protected].
494
springs, the deep sea, desert ponds, and waters with
little to no oxygen.
This symposium united microbiologists, physiologists, and evolutionary biologists to present cutting
edge research representing the breadth of extremophile biology. The first recognized extremophiles
were microorganisms living at high temperatures
(thermophiles) or in high salt concentrations (halophiles) and it was not until the last half of the 20th
century that life was also found in highly acidic environments (acidophiles), under extreme pressures
(piezophiles) and frozen in ice (psychrophiles),
among others (Morita 1999). While the term ‘‘extremophile’’ was originally used to describe microbes
(Macelroy 1974), all domains of life are now recognized to inhabit extreme environments. Symposium
speakers discussed a number of these highly novel
organisms that span the breadth of taxonomy, from
an apicomplexan acidophile Nephromyces which
resides in the renal sac of ascidian tunicates (Saffo
et al. 2010) as presented by Chris Lane, to microbes
that reside in Antarctic subglacial lakes as presented
by Jill Mikucki (Mikucki et al. 2015), to deep sea eels
with complex migratory routes as presented by
Shannon DeVaney (DeVaney et al. 2016).
Historically, little has been known about the biology
of extremophiles due to the inaccessibility of their
habitats. Recent advances in sampling technology,
concerns over climate change and renewed interest
in extreme habitats such as the deep sea for industrial purposes, have helped begin to improve sampling capability. Additionally, as new methodologies
such as high-throughput sequencing have become
readily accessible, more information can be obtained
from the samples collected, uncovering mechanisms
by which organisms are capable of not only surviving, but also thriving, in extreme ecosystems. Below
we highlight a breadth of taxonomic groups inhabiting extreme habitats including those with high or
low temperatures, high pressures, and/or little to
no oxygen.
Microbes and viruses
Deep-sea and terrestrial hydrothermal environments
provide a rich diversity of novel thermophilic and
hyperthermophilic
Bacteria
and
Archaea.
Hydrothermal systems represent one of the most
chemically diverse habitats for microorganisms. In
terrestrial hydrothermal systems, the presence of
light allows for a photosynthetic extremophiles, in
addition to heterotrophs and chemolithotrophs, to
thrive in hot springs. However, at deep-sea vents
the microorganisms derive their energy not from
A. R. Lindgren et al.
the sun, but from geochemical fluxes from Earth’s
interior (Jannasch and Wirsen 1979). Primary productivity at vents occurs as chemolithoautotrophic
microbes fix carbon by oxidizing reduced chemicals
in vent fluids (e.g., reduced Fe, Mn, H2(aq),
H2S(aq)) with a variety of electron acceptors in sea3þ
water (e.g., oxygen, SO¼
4 , NO3, and Fe ) (Jannasch
1995). The vent deposits form by mineral precipitation as hot, reduced, and metal-enriched hydrothermal fluids are emitted on the seafloor, and the walls
of these structures form permeable matrices that
allow a gradual mixing between hydrothermal
fluids flowing upward through the center of the
vent and surrounding seawater. The vent walls span
temperatures from 2ºC to4400ºC and provide one
of the few environments on Earth for searching for
the upper temperature limits of life (e.g., Baross and
Deming 1983). Over the past decade or so, much of
the microbial diversity associated with actively venting hydrothermal deposits has been described using
16S rRNA gene cloning approaches (e.g., Takai et al.
2006 and references therein). Advances in culturing
approaches (e.g., for review, Stetter 1999 among
others) have resulted in many new descriptions, continuing to challenge our understanding of extremophiles and biological processes never previously
detected at deep-sea vents (e.g., Reysenbach et al.
2000, 2006; Flores et al. 2011; Slobodkin et al.
2013). High-throughput sequencing technologies
and metagenomics have revealed differences in the
microbial communities within and between vent
fields on a global scale which appear to be driven
in part by differences in vent fluid composition, including pH (Flores et al. 2011, 2012). Anna-Louise
Reysenbach’s oral contribution to the symposium
discussed how metagenomics could be utilized to
investigate metabolic pathways used by archaeal
and bacterial extremophiles and to look for indicators as to how the physical environment impacts
community assembly from a genomic perspective.
Bacteria, and Archaea in particular, inhabiting extreme environments are commonly infected with
novel viruses with unique morphologies (Pina et al.
2011). For instance, bottle- and spindle-shaped viruses that change morphology depending on environmental conditions (Häring et al. 2005a, 2005b).
Genome packaging is also unique; positively supercoiled DNA in the Sulfolobus spindle-shaped virus
SSV1 (Nadal et al. 1986) and A-form DNA in the
Sulfolobus islandicus rod-shaped virus SIRV2
(DiMaio et al. 2015). These unique DNA packaging
mechanisms likely help stabilize the DNA under extreme conditions. A new pyramidal pore for virus
release was found in SIRV2 and STIV infected cells.
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Biology of organisms inhabiting extreme environments
The majority of genes in extremophile virus genomes
are also unique (Pina et al. 2011), suggesting that
there are many new and exciting features of these
viruses to be discovered.
Plants
In the majority of extreme terrestrial environments,
cryptogams (lichens, bryophytes and algae) are the
dominant plant species. Cryptogams survive well
with high and low water availability and at high
and low temperatures (Cornelissen et al. 2007), and
occur in communities from the arctic and Antarctica,
to geothermal hot springs, and the world’s most extreme deserts. Species-specific physiological responses
have been found to explain bryophyte and lichen
species’ ability to survive in the most extreme environments (e.g., Llaneza Garcı́a et al. 2016; Raggio
et al. 2016), and species-specific physiological effects
must be included in modeling of the effects of climate change on extreme environments. These extreme systems are rarely nutrient-limited (Robinson
et al. 2003), however, global climate change is likely
to alter these conditions making nutrient limitation
and competition with vascular plants more prevalent,
and in some extreme environments, such as the polar
systems, cryptogam populations are beginning to decline (e.g., Elmendorf et al. 2012; Bokhorst et al.
2016).
Vascular plants are not absent from extreme environments and recent research suggests that interactions with microbes are critical to these plants’ ability
to survive in the most extreme environments such as
geothermal hot springs, serpentine soils, and mine
waste sites. Marquez et al. (2007) found that a
three-way interaction among a grass (Dichanthelium
lanuginosum that grows around Yellowstone hot
springs), a fungal endophyte (Curvularia protuberate), and a virus allows thermal tolerance. Fungal
endophytes have been found to confer heat and
salt tolerance to native grass species (Rodriguez
et al. 2008) and heavy metals tolerance to native
forb species (Sun et al. 2010). Vascular plants’ interactions with mycorrhizal fungi also allow survival in
environments with extreme temperatures (Bunn
et al. 2009; Zhou et al. 2015), high salt (ReussSchmidt et al. 2015), and severely low water and
nutrients (for review Smith et al. 2010). Endophytic
bacteria and rhizobacteria have been found to greatly
enhance plants’ ability to survive in environments
with heavy metals, such as mine sites (e.g.,
Dell’Amico et al. 2008; Chen et al. 2014).
Invertebrates
Invertebrates from a diverse array of phyla occupy
extreme environments in the marine realm where
they are often dominant members of the community.
In the deep sea, high pressures combine with high or
low temperatures, respectively to create some of the
most physiologically stressful conditions on Earth
Inhabitants tend to have a reduced metabolism, irregular spawning periods (Ramirez-Llorda et al.
2010), and possess biochemical adaptations to overcome the physiological stress of living under extreme
pressures (Somero 1992). At hydrothermal vents,
many marine invertebrates engage in symbiotic associations with chemoautotrophic microbes, most
commonly to take advantage of primary productivity. Although host physiology is often invoked as the
main factor influencing distribution, Roxanne
Beinart’s oral contribution emphasized the important
role endosymbionts play in driving community
structure and habitat partitioning based on vent geochemistry (Beinart et al. 2012).
At the opposite end of the thermal spectrum and
outside of the influence of extreme pressure are the
near-freezing temperatures in the shallow polar waters.
Marymegan Daly (see also Daly et al. 2013) presented
information on a recently discovered species of
Antarctic sea anemone Edwardsiella andrillae which
lives upside-down, embedded in the ice with its numerous tentacles waving into the water below. While
the original sample material was insufficient to provide insight into how these anemones burrow into
and survive in glacial ice, recent additional sampling
and study continues to yield new insight into their
biology and physiology. For example, Murry et al.’s
(2016) contribution to the symposium discusses the
impacts the microbiome may have on freezing avoidance in the Antarctic sea anemone E. andrillae.
In the open ocean, one of the most challenging
areas to inhabit are oxygen minimum zones, widely
distributed naturally occurring areas where oxygen
levels are often less than 0.15 ml/l (51% saturation)
often associated with areas of high primary productivity, such as seen in the eastern tropical Pacific
(e.g., Childress and Seibel 1998). The presence of
low oxygen levels characteristic of OMZs impact
the distribution and ecology of marine animals
who cannot survive hypoxia (oxygen deficiency) for
even a short period of time; zooplankton biomass is
significantly lower in the OMZ than surrounding
oxygenated waters and the resident predators spend
prolonged periods of time migrating vertically to
oxygenated waters (e.g., Rosa and Seibel 2010).
496
While overall diversity is reduced in OMZs, some
taxa
including
squids,
the
cephalopod
Vampyroteuthis infernalis and euphausiid crustaceans
have proven successful at tolerating hypoxic stress
(Brinton 1979; Rosa and Seibel 2010; Hoving and
Robison 2012). Seibel et al.’s (2016) contribution
to the symposium discussed the effects living in
oxygen minimum zones have on organisms from
squids to euphausiids, suggesting that metabolic suppression is a key strategy vertical migrators use when
spending time in areas of low oxygen. The oxygen
minimum zones are thought to be expanding, both
vertically and horizontally (Stramma et al. 2008),
making their inhabitants model organisms for understanding if/how other organisms will be able to compensate for decreases in oxygen levels.
Fishes
Many vertebrate species, often with complicated physiologies and life histories, thrive under conditions
that would be prohibitive for their closely related
cousins from moderate habitats. Good examples include both ectotherms such as desert lizards and insects and endotherms such as high altitude
mammals, hibernators and polar birds and marine
mammals. Fishes however, are capable of surviving
in many habitats intolerable to other vertebrates,
from the freezing polar oceans to desert ephemeral
ponds. The fishes of the polar oceans are excellent
examples of life as it exists in the extreme cold:
Arctic and Antarctic fishes display many molecular,
cellular, physiological, and organismal specializations
that allow them to flourish in cold waters.
Alternately, survival in unpredictable, hot, isolated,
and temporary habitats, such as desert ephemeral
ponds, presents a unique test for fishes: unable to
migrate to more favorable conditions, they must tolerate the harsh environment until conditions are
once again favorable. Below, these two ends of the
physiological spectrum are discussed in greater detail.
Polar ocean fishes
The Antarctic fishes conduct physiological ‘‘business
as usual’’ in waters that are constantly near or below
0 8C. Many Antarctic fishes lack a traditional heat
shock response, wherein the rapid up-regulation of
heat shock proteins (Hsps) follows exposure to heat
stress in order to chaperone thermally damaged proteins (Hofmann et al. 2000; Buckley et al. 2004; Place
and Hofmann 2005; Clark et al. 2008; Buckley and
Somero 2009). Instead, these species produce Hsps
constitutively, presumably to mediate the routine
folding of proteins in the cold (Place and
A. R. Lindgren et al.
Hofmann 2005; Todgham et al. 2007; Buckley and
Somero 2009; Thorne et al. 2010; Bilyk and Cheng,
2013). Antarctic fishes also display an elevated level
of expression of genes involved in protein degradation through the ubiquitin pathway (Buckley and
Somero 2009; Shin et al. 2012).
Other notable features of the transcriptomic response of Antarctic fishes to elevated temperatures
include the up-regulation of oxidative stress response
genes as well as genes encoding proteins involved in
inflammatory responses (Thorne et al. 2010; Huth
and Place, 2013; Windisch et al. 2014). These observations support the idea that despite losing the ability to adaptively modify the expression of Hsps, these
fishes have maintained the ability to respond to
warming waters. In addition, genes involved in cell
cycle arrest and apoptosis are inducible in these coldadapted species, suggesting that in the absence of an
inducible heat shock response, interruption of cell
division and/or cell cycle arrest are favored
(Buckley and Somero 2009; Sleadd et al. 2014).
Antarctic fishes live in some of the coldest, most
well oxygenated waters on Earth and as our planet
warms and the climate becomes more variable and
unpredictable, a focus on the biology of polar ectotherms will only become more important. Brad
Buckley discussed how the loss of well-conserved responses such as the up-regulation of Hsps may favor
other cellular mechanisms of response (Buckley and
Somero 2009) during exposure to elevated temperature and O’Brien et al.’s (2016) contribution to the
symposium discusses how the oxygen-rich waters of
Antarctica have facilitated the loss of oxygen-binding
proteins in these fishes.
Ephemeral pond fishes
One of the most well-known examples of aquatic
vertebrates that tolerate variable environmental conditions are the annual killifish from ephemeral ponds
(Myers 1952). Found exclusively in regions of South
America and Africa, annual killifish live in ponds
with daily fluctuations reported to reach over 1 pH
unit and a temperature range of 26–37.5 8C
(Podrabsky et al. 1998). Over the past two decades,
these fish have emerged as a model for studying extreme stress tolerance in vertebrates. One of the early
studies utilizing cDNA microarray analysis of mRNA
expression found that adults of the annual killifish
Austrofundulus limnaeus were able to stabilize their
gene expression patterns following a several weeks of
temperature cycling from 208C to 37 8C (Podrabsky
and Somero 2003). While the ability of adult annual
killifish to tolerate and acclimate to fluctuating
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Biology of organisms inhabiting extreme environments
conditions is impressive, permanent populations persist only because of the production of stress-tolerant
embryos that survive seasonal desiccation. Embryos
are characterized by their ability to arrest development at one to three stages of embryonic development, with the most stress-resistant stage occurring
approximately midway through development, at a
stage known as diapause II (DII) (Wourms 1972).
As they develop buried in sediment, A. limnaeus embryos have the highest known tolerance of anoxia of
any known vertebrate and respond to acute anoxia
exposure by rapidly entering into a state of quiescence (Podrabsky et al. 1998, 2007). Podrabsky and
Wilson’s (2016) contribution to the symposium discusses the how interplay between increased temperature, the stage at which embryos enter diapause,
and their ability to tolerate anoxia all affect the duration and success of development in annual killifish
living in ephemeral ponds.
Future directions
In discussing extremophiles from diverse taxonomic
and ecological backgrounds, several interesting
themes emerged in this symposium. The first is the
ubiquity and diversity of symbiotic associations
among extremophiles. Here, we have highlighted
some of the cases in which plants and invertebrates
engage in symbiotic associations with microbes that
appear to help mediate stressors associated with
living in an extreme environment. However, much
of what we know about the role symbioses play in
extreme conditions remains elusive, due difficulties
in culturing or quickly sampling microbiota from
extremophilic eukaryotes, which leads to the second
theme that emerged from this symposium: sampling
and studying extremophiles is very challenging. So
much remains to be learned about extreme ecosystems, but the majority are costly and lengthy to
reach. Researchers working in these areas often face
harsh conditions and collection planning and subsequent data gathering must be maximized. Speakers
from this symposium were united in the need for
additional sampling, which will continue to yield
novel insight into the how life persists under extreme
conditions. The last, but likely most important,
theme that emerged from this symposium is the
role extremophiles play in understanding how life
will respond to a changing climate, in terms of
both temperature and oxygen. Organisms that live
under anoxic conditions, or require maximally
oxygen-saturated waters are particularly susceptible
to increases in temperature. As temperatures increase, so do metabolic demands, which can make
the strategy of utilizing metabolic suppression to
manage oxidative stress particularly challenging.
Whether it is fish living in freezing waters, cephalopods in oxygen minimum waters, or embryos living
without oxygen at high temperatures, extremophiles
are the both the ‘‘canary in the coal mine’’ and the
best indicators we have for how life will respond to
climate change. Research into extremophiles and
their biology remains in its infancy, and as we explore this planet more, especially in difficult to reach
and thus under sampled areas, many more discoveries of the extremes of life will continue to emerge.
Funding
Support for participation in this symposium was
provided by the Society for Integrative and
Comparative Biology and its Division of Physiology
and Comparative Biology and by the National
Science Foundation (IOS 1546672). Research pertaining to this publication was supported by the following NSF grants: PLR 1341742 (SME), MCB
1243963 (KMS), ANT 0944743 (BAB), and OCE
123542 (ALR).
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