Article type: Opinion
Article title: A Germ Theory for Glacial Systems?
Authors:
Full name and affiliation; email address if corresponding author; any conflicts of interest
First author (corresponding)
Arwyn EDWARDS aye@aber.ac.uk
AU Interdisciplinary Centre for Environmental Microbiology & Centre for Glaciology,
Institute of Biological, Environmental & Rural Sciences (IBERS) Aberystwyth University
Second author
Tristram IRVINE-FYNN
AU Interdisciplinary Centre for Environmental Microbiology & Centre for Glaciology,
Department of Geography & Earth Sciences (DGES) Aberystwyth University
Third author
Andrew C. MITCHELL
AU Interdisciplinary Centre for Environmental Microbiology & Centre for Glaciology,
Department of Geography & Earth Sciences (DGES) Aberystwyth University
Fourth author
Sara M.E. RASSNER
AU Interdisciplinary Centre for Environmental Microbiology & Centre for Glaciology,
Department of Geography & Earth Sciences (DGES) Aberystwyth University
Abstract
Glacial systems in the form of glaciers and ice sheets are important actors in Earth’s water cycle and
climate. Improving our understanding of their structure and functionality is of considerable
importance, and glaciologists have tended to apply a purely physical perspective to the study of
glacial systems. However, a novel paradigm of glaciers and ice sheets as Earth’s largest freshwater
ecosystems is being supported by studies revealing the abundance, activity and diversity of life in
glacial ecosystems and the importance of glacial systems in global biogeochemical cycles.
Nevertheless, while the importance of microbial activities in shaping their habitats and influencing
landscape-scale processes is well recognized elsewhere in our biosphere it has hitherto been
overlooked in glacial systems. Here, the potential for several discrete microbial processes to interact
with mass balance and landscaping in glacial systems as part of a “germ theory” of glacial systems is
identified. These processes range from microbial biocatalysis of ice crystal formation and structure,
albedo reduction by microbial assemblages at the ice-atmosphere interface to microbe-mediated
mineral weathering at the rock-ice interface. Integrating these microbial processes with abiotic,
physical processes in a framework of microbial glaciology will be required to understand the extent
and significance of microbial influences upon the properties of glacial systems. Furthermore,
adopting a microbial glaciology approach also complements existing physical and chemical
approaches to glaciology to understand how glacial systems respond to our warming climate.
Introduction
The role of the infinitely small in nature is infinitely great.
Louis Pasteur
Presently, glacial systems, comprised of glaciers and ice-sheets, occupy 11% of Earth’s surface area
and harbour approximately 70% of the surface stores of freshwater1. Our planet has been subjected
to repeated glaciations throughout its geologic history, including five major glaciations in the last
500,000 years2 and even a pervasive Neoproterozoic glaciation terminating prior to the Cambrian
radiation around 600Ma BP3.
The importance of glacial systems with respect to contemporary climate change is also evident. It is
anticipated that for every degree of climate warming, sea levels will rise 2.3 metres over the next
2000 years4, and ice sheets are predicted to contribute up to a metre to sea level rise this century5
resulting in the displacement of up to 190 million humans6 from heavily populated and agriculturally
important coastal areas 7. Furthermore, changes in melting risk affecting a billion people whose
water security is underpinned by resources from glacierized catchments8. Therefore, it is clear that
glacial systems are critical components in the Earth system at timescales from the societally-relevant
to geologic and evolutionary, and that understanding processes affecting glacial systems assumes
considerable contemporary relevance.
However, the biology of glacial systems has been poorly considered until recently. Kohshima9 first
identified a simple glacier-associated food web and introduced the notion of a glacial ecosystem in
1984. However the concept that glacial systems harbour microbially-dominated ecosystems was
only consolidated by the landmark review by Hodson et al.10 of glacial ecoystems published in 2008.
This has led to calls to recognize glacial systems as a discrete biome11 and the importance of
microbial activity at the surface of glacial systems12.
The belated nature of these discoveries most probably stems from the predominantly microbial and
hence invisible nature of these ecosystems. Although Pasteur was the first to demonstrate that
important processes are mediated by microbes, specifically by means of his germ theory of disease
causation, our understanding of how “the role of the infinitely small in nature is infinitely great”13 is
still incomplete. Nevertheless, we must now appreciate that Earth’s poorly catalogued14 “microbial
majority” 15 drives its biogeochemical cycles16 and hence assumes a crucial role in the functioning of
the biosphere. Furthermore, since microbes in cold region ecosystems can act as both “sentinels and
amplifiers” of climate change17 it is pertinent to consider the potential scale and significance of the
glacial biome.
The extent of the glacial biome remains poorly defined, but we18 recently estimated that glacial
systems harbour between 4×1025-7×1029 bacterial or archaeal cells and that up to 1×1026 reside in
the uppermost 1-2 metres of ablating glacier ice areas. Additionally, microbes are abundant at the
glacier bed19. Both supraglacial and subglacial environments support microbial life. For instance, the
surface ice layer experiences seasonal melting and penetration of sunlight, thus providing conditions
most conducive to microbial activity and is consequently considered a glacial photic zone.
Surprisingly, our estimate of cell abundance in the global glacial photic zone compared remarkably
well with the estimated cellular abundance of the global oceanic photic zone, or the bacterial and
archaeal abundance of all rainforest soils15. If microbial life at the surface of glacial systems alone is
as abundant as that of a habitat which accounts for half of global primary production20, the lacunae
in our understanding of the importance and parameters of microbial processes in the glacial biome
must be remedied.
Our objective in this article is to evaluate the functionality of the glacial biome by examining biotic
interactions with glacial systems[FIGURE 1]. In doing so, we reflect upon Pasteur’s comment and ask
whether the role of the infinitely small in glacial systems is perhaps infinitely great. Therefore we
focus upon our current understanding of microbial contributions to fundamental glacial processes.
We identify several discrete microbial processes which interact with glacial mass balance and
landscaping and thus lead to the argument that microbes have the potential to influence key aspects
of the properties of glacial systems. We refer to this microbial influence upon glacial systems as a
“germ theory of glacial systems” and consider whether a microbial approach to glaciology should be
considered.
MICROBIAL INTERACTIONS WITH GLACIAL MASS BALANCE
Glacial systems function as a consequence of the perennial accumulation of snow, its
metamorphosis to plastic glacial ice, its subsequent deformation and flow to lower elevations, where
through melt or sublimation the ice ablates. The net balance between the extents of ice mass gain
(accumulation) and loss (ablation) is known as the mass balance, and is positive if the former
exceeds the latter or negative if vice versa. Hitherto, the factors known to affect the mass balance
of glacial systems are typically characterised as abiotic in nature, and contingent upon purely
physical processes. However, in contrast, there are multiple microbial processes which can interact
with accumulation and ablation processes, and hence glacial mass balance.
Microbes and Accumulation
Every glacier starts with a single snowflake. Correspondingly, there are biological contributions and
interactions in the formation of atmospheric ice crystals. Since Pasteur’s initial investigations of
alpine glacier aerobiology13, the role of the atmosphere in dispersing microbes to glacierized regions
is well recognized. Indeed, the atmosphere is not merely a conduit for the passive transport of viable
microbes in a dormant state21 as evidence for metabolic activity in supercooled growth droplets has
been found22. Microbes capable of growth at timescales, temperatures, and upon nutrients typical of
cloud habitats have been isolated from cloudwater23 and hailstones 24. Although ice precipitation
supports the deposition of microbes into snowpacks25, it is likely a coherent process26 with microbial
processes contributing to accumulation itself via “bioprecipitation”27 where biotic agents act as
nuclei which initiate ice crystal formation.
Microbial catalysis of ice nuclei formation was first identified in the 1970s28. Ice-nucleating bacteria
such as the Gammaproteobacterium Pseudomonas syringae promoted freezing at higher
temperatures, approaching 0°C, than abiotic controls freezing at -40°C. Furthermore, there have
been arguments that biological ice nucleators (IN) appear to influence the water cycle26. While the
extent of biological IN in global precipitation may be open to question29, Christner et al.30 found
abundant biological IN activity in fresh samples of snowfall collected in Antarctica, Europe and North
America. Heat inactivation reduced 69-100% of IN activity while lysozyme reduced 0-85% of IN
activity, leading to the inference that biological IN, and in particular, cell-associated (enzyme) IN
activity contributed by a small fraction of the cells present (<0.5% of the population) was responsible
for much of the ice nucleation occurring at ambient temperatures of snowfall30, 31.
It may be assumed that this geographically diverse snow sample set30, 31 is broadly representative of
the bacterial communities of snowfall in glacierized regions on the grounds that cosmopolitan
lineages of bacteria are present in snow32 and that IN activity is a phenotype facilitating dispersal of
bacteria26. Therefore it is likely that a microbial process exerts an important influence in the snowfall
inputs which nourish the accumulation zones of glacial systems.
The accumulation zones of glacial systems themselves are now acknowledged as microbial habitats.
Precipitation-associated (“wet”) deposition as described above as well as “dry” (aeolian-associated)
deposition introduces microbes to glacial accumulation zones25. The microbial assemblage of glacial
snowpacks could be viewed as the integration of microbes deposited by both mechanisms across a
continuum from atmosphere to snowpack, but with a discontinuity arising at the interface between
the snowpack and glacier ice32.
It appears that the snowpack is home to active microbial communities, which may influence surface
albedo (for instance red-pigmented snow algal blooms33), and are active even in ‘dry’ snowpacks34
free of liquid water. Glacier surface snowpack communities are temporally variable, even at brief
(week-long32) timescales in response to melting. On High Arctic glaciers it appears slush, as the
decomposition product of snow which harbours a distinct and highly dynamic bacterial community32
dominated by members of the Betaproteobacteria.
Hell et al.32 suggested that a betaproteobacterial-dominated slush community could bloom in
response to spatially-extensive episodic melting events, such as that observed on the surface of the
Greenland Ice Sheet in 2012 35. However the fate of cells growing in such a bloom is unclear, as other
influences (e.g. dry-deposited cells) and elution in runoff may disrupt its entombment in firn and
glacial ice. Nevertheless, the discovery on Greenland of an extensive perennial store of meltwater as
slush in firn36 may provide a stable microbial habitat. Further work is required on the dynamics of
microbial communities during the densification of snow and the formation of glacial ice, but the
eventual formation of glacial ice crystals creates three microbial habitats within a glacier. These are
comprised of intercrystalline brines, ice-mineral interfaces and even inside ice crystals, the latter
potentially as the result of small gas molecule diffusion permitting metabolism of carbon dioxide and
methane in deep glacial ice37-39. Microbes producing ice-binding (IB) proteins which inhibit the
recrystallization of glacial ice40 have been recovered from a depth of 3519 metres within the Vostok
ice core. Expression of these IB proteins improves the fitness of bacteria exposed to freeze-thaw
stresses 41. Bacterial control of ice crystal structure by IB proteins thus offers an adaptation
supporting longevity in glacial ice, incurring structural implications and potential rheological
consequences for microbial catalytic reordering of the crystalline ice matrix41 by IB proteins.
In summary, microbes interact with ice crystals via IN and IB proteins, and thus the interactions of
microbial communities present in snowfall, slush, and glacial ice with ice crystals have the potential
to influence the properties of glacial systems. Biocatalytic interactions with ice crystals may even
predate IN and IB protein evolution given recent evidence of in-ice evolution of ribozyme
biocatalysis in intercrystalline spaces42. Since in-ice ribozyme biocatalysis raises the spectre of a
glacial origin for life42 the scope and evolutionary intimacy of biocatalytic interactions with ice
crystals in glacial systems may be much greater than readily apparent.
In the Ablation Zone
At the lower elevations of glacial systems, the rate of ablation exceeds accumulation, resulting in ice
mass loss primarily through sublimation and melting. The genesis of meltwater promotes conditions
conducive to life, particularly when coupled with incident sunlight. Ablation is not limited to the iceatmosphere interface, but includes losses at the crystal boundaries in the near-surface ice.
Consequently, the ablation zones of glacial systems support life upon and within a “weathering
crust” of ice seasonally affected by surface melt and ablation processes. As outlined above, this icesurface habitat comprises a glacial photic zone18 but presents something of a paradox. The seasonal
cell budget of a High Arctic glacier reveals that as ice mass ablates, microbial biomass accumulates;
at higher discharge levels, cellular intercrystalline mobility is impeded43. The retention of microbial
biomass is thus proportional to melting rate. With the net gain of microbes and other particulates
deposited or emerging at the surface this can result in “biological darkening” of the surface43. This
darkening has significant implications for glacier surface energy balance, and hence melting rates
themselves [FIGURE 2].
The most striking manifestations of biological darkening are macroscopically-visible microbe-mineral
aggregates known as cryoconite44. These occur as a consortium of diverse life forms colonizes
allocthonous organic and mineral aeolian deposits on the ice surface. The metabolism and
agglomeration of dark organic matter within cryoconite aggregates 45 reduces the local albedo and
promotes preferential melting of the ice. These processes are closely associated with the microbial
community. Cyanobacteria act as keystone taxa, engineering the cryoconite ecosystem 46, 47 for
heterotrophic taxa such as Proteobacteria and fungi 48-50 as a microbial community distinctive from
proximal habitats assembles49, 51.
Preferential melting as a consequence of organic matter agglomeration within cryoconite aggregates
leads to the formation of pot-hole like structures known as cryoconite holes which tend towards an
equilibrium depth determined by prevailing meteorological conditions 52. Within cryoconite holes,
aggregate motion is controlled by local synoptic and hydrological conditions53. Thermodynamic
processes promote the lateral re-distribution of aggregates54 to achieve an aggregate monolayer.
Such an aggregate monolayer maximises ecosystem productivity 54 and a tendency to net autotrophy
55
by Arctic cryoconite. Moreover, cryoconite microbial community structure and activity is
associated with surface hydrology 49, 50 and the composition of cryoconite organic matter47. As such,
interactions between cryoconite microbial processes and hence its properties and surface melting
are likely 50, providing a biotic positive feedback loop in glacial system ablation. Our observations are
biased to Northern hemisphere glaciers rather than the entombed, hydrologically-isolated
cryoconite ecosystems found on colder Antarctic glaciers, yet cryoconite on Antarctic glaciers can
still contribute substantially to meltwater runoff56.
A focus solely on cryoconite ecosystems risks neglecting the importance of other surface habitats in
the ablation zone. Ignoring photosynthesis by specialist ice algae risks underestimating supraglacial
carbon fixation on Greenland by an order of a magnitude 57. Unlike cryoconite aggregates which may
be self-shaded55 and protected by residence at equilibrium depth52, ice algae, being situated atop
the ablating ice column are less shielded from extremes including harmful light intensities57.
Correspondingly, while their rates of photosynthesis per unit biomass can be lower than cryoconite,
their impact is magnified by extensive areal coverage57, 58. In turn, ice algal pigmentation, in part as a
photoprotective mechanism, can reduce albedo. Furthermore, ice algae will interact with the
ablating ice surface under a broader range of synoptic hydrometeorological conditions than
cryoconite59. In western Greenland, Yallop et al58 demonstrated both a relationship between algal
coverage and albedo, and micro-scale algal albedo reduction exceeding that from mineral particles.
As the extent of carbon fixation by ice algae is predicted to increase with the extent and duration of
bare ice due to climate warming, the influence of ice algal biomass on surface melting is set to
increase with warmer climate 57. Since transfer of organic carbon between habitats via aeolian and
melt-related processes around the ice surface occurs 60, accumulation of dark organic carbon by
distinct consortia of microbes, ice algae and cryoconite, respectively, potentiates a synergistic
feedback of biomass accumulation and thus exerts an important influence on ice albedo. Microbial
biomass is already evident in the emergence of expansive “dark regions” at the Greenland ice sheet
margin61. Attributing the extent of microbial contributions to ice albedo relative to other ice surface
impurities is a research priority62.
MICROBIAL INFLUENCES ON GLACIAL GEOMORPHOLOGY
The interface between rock and glacial systems is a powerful engineer of landscape (e.g.63). Indeed,
glaciers can be thought of as “factories” generating reactive mineral surfaces64. Permanently dark
and cold, it was thought any life at the glacier bed would be caught between rock and a hard place,
and thus subglacial environments were considered essentially sterile. Reports of abundant and
active subglacial bacterial populations in 1999 and 200019, 65 shifted this paradigm. Fifteen years later
it is accepted that subglacial till and debris-rich basal ice66environments are home to endogenous67
active microbial populations 68, in particular where ice resides above its pressure melting point thus
permitting water to be liquid69. Subglacial cycling of carbon and macronutrients is evident 70 and
subglacial methanogenesis is of particular concern. The rate of production of methane by subglacial
Archaea71 appears influenced by the bioavailability of organic carbon overridden during glacial
advances72. Numerical simulations suggest that the quantity of methane hydrate currently
sequestered beneath Antarctica may be in the same order of magnitude as Arctic permafrost73.
Consequently, subglacial methanogenesis is thought to represent a potential positive feedback in
climate warming74 unless compensated for by other processes.
Since permanent darkness prevents photosynthesis as a source of energy, the importance of
microbially-mediated lithotrophic redox reactions in subglacial ecosystems is inferred65, 75 from
multiple lines of evidence, for example the presence of 16S rRNA sequences related to known
lithotrophic microbes67, 68, 76. Moreover, experiments using in situ incubations of different minerals
reveal bedrock mineral composition as a driver of bacterial community structure and biomass
formation77. The importance of subglacial microbial processes as a primary driver of subglacial
chemical weathering75 has been confirmed recently using laboratory models78. Incubations of basal
sediments with active and killed indigenous microbial communities revealed biotic processes which
typically promoted weathering rates eight fold78. The fold-increase in the release of different ions
varied according to cation, and in particular due to catchment, but overall the experiments provide
strong support for inferences from field observations75, 79. As such, it seems likely that subglacial
microbial processes strongly interact with glacial comminution80 to influence bedrock mineral
dissolution and the corresponding composition of cognate meltwaters. Transfer of the products of
subglacial microbial weathering to downstream ecosystems assumes a particular significance,
perhaps best exemplified by the role of bioavailable iron and other biologically significant trace
elements liberated by subglacial biogeochemical processes in fertilizing iron-limited coastal oceans81.
Finally, microbial geomorphic82 processes continue to play important roles in the terrestrial forefield
of glaciers. Glacier forefields have long been considered textbook examples of “macrobial”
ecosystem development by primary succession (e.g.83). Similar processes appear at play in the
microbial colonization of glacier forefields84, but influences from inoculation of microbes from glacial
communities are less well considered. Regardless of their source, it is apparent microbes in glacier
forefields are also active in mineral weathering85-87, and microbially-mediated weathering promotes
the development of microbial and plant biomass 88. The accumulation of microbial biomass, typically
in biological soil crusts, itself acts to stabilize sediments and promote the retention of organic
matter89, 90. Consequently, microbial geomorphic processes conducted by pioneering microbes
associated with glacial systems are active in depositional environments and modes as well as in loci
of erosion such as subglacial ecosystems82.
Conclusion
Glacial systems are Earth’s largest de facto freshwater ecosystems in terms of their volume and are
abundant in microbial life18. The roles of glacial ecosystems in global biogeochemical cycles are now
recognized73, 81, 91. This article aimed to present a number of discrete microbial processes occurring in
glacial systems contributing to snow accumulation, ice ablation, mineral weathering and the
evolution of proglacial environments. It is abundantly clear that microbes are geobiological agents
capable of interaction with, and ultimately, the engineering of their habitats throughout our
biosphere. We contend that transferring these concepts to glacial systems unify the disparate
microbial processes considered herein as a germ theory of glacial systems. Furthermore, the extent
to which microbial processes shape the structure and function of glacial systems must be
considered.
Recognizing microbial contributions to glacial systems dynamics does not nullify the importance of
well-studied abiotic, physical processes acting upon these systems. For instance, although glacial
systems on other planets may differ radically in their accumulation, ablation and modes of flow
compared to glaciers on Earth92 it is clear that their existence is not contingent on biological
processes. Thus, if Martian glacier-like forms represent an abiotic end-member in a gradient of
biological influence upon glacial systems, determining where the glacial systems present on Earth
reside upon that gradient is a priority.
Clearly, understanding the relative importance of biological processes to the structure and function
of different glacial systems will require further investigation. Chief among these will be (i) the
quantification of microbial biocatalytic interactions with ice and their consequences for
accumulation and rheology (ii) attribution of impacts from biological darkening upon glacier albedo
relative to other impurities on glacier surfaces and (iii)understanding microbial interactions with
mineral surfaces in different catchments with contrasting subglacial physical and mineralogical
conditions. Regardless of the merit of a germ theory for glacial systems, such investigations within
the domain of a “microbial glaciology” will provide vital information to complement insights from
physical glaciology and glacial geochemistry in understanding how Earth’s glacial systems will
interact with its warming climate.
Acknowledgements
The authors are grateful for the support of the Research Capital Investment Fund of the Higher
Education Funding Council for Wales in developing the interdisciplinary Centre for Environmental
Microbiology. Current research on glacier microbiology by the authors is funded by grants from
NERC (NE/K000942/1) and the Royal Society (RG2013) to AE, EU FP7 (InterAct SCARFACE) to TI-F &
AE, US NSF (WISSARD-GBASE 0838933) to ACM and the Freshwater Biological Association Hugh Cary
Gilson award to SMER, TI-F & AE. Finally, the authors are grateful for the assistance of Antony Smith
in developing Figure 1 and the reviewers and editor for their constructive comments.
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Figure captions
FIGURE 1: A Germ theory of glacial systems? A conceptual overview of microbial habitats and
processes in an idealized glacial system. Based upon a figure from Irvine-Fynn, (2008), unpublished
Ph.D. thesis, Sheffield University.
FIGURE 2: The ice surface habitat illustrating biological darkening by cryoconite and the glacial photic
zone. Note the effects of discrete cryoconite holes and dispersed cryoconite material residing at the
ice surface on the spectral response of ice relative to bare ice (dashed line) or meltwater on bare ice.
The glacial photic zone is viewed in transverse as a porous ice layer perched atop less permeable ice,
presenting a microbial habitat in receipt of dissolved nutrients and sunlight. This figure is reproduced
from Reference 13 by permission.
Further Reading/Resources
Laybourn-Parry, J.; Tranter, M.; & Hodson A.J. (2012). The ecology of snow and ice environments.
Oxford University Press, UK.
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