**6. Microorganisms in retreat glaciers**

Global warming is having a great impact on glaciers, because of the change in air temperature and precipitation [48, 49]. Glacier retreat directly affects various atmospheric, climatic, and ecological phenomena. In retreat glaciers, the thickness of ice and snow decreases, and fossil ice emerges, forefield surface increases (**Figure 4**), new soil develops; and they are colonized by new prokaryotic and eukaryotic microbial species.

vein habitat provides water, energy, and nutrients. In contrast with this, the metabolism of microbes encased in solid ice must overcome the diffusion of nutrients in a solid media [36]. Microorganisms in englacial ecosystems can be chemoautotrophs, but they can also be heterotrophic bacteria that feed on solubilized products from pollen grains, invertebrates, and other microorganisms. At great depth, anaerobic respiration can take place [35, 37], and methano-

At glacial sediments and bedrock, debris contains minerals and sedimentary organic carbon that, combined with subglacial water, create microniches where microorganisms can live [5]. A strong coupling is likely to exist between the hydraulic conditions at the glacier bed and the bacterial processes that take place [20]. The subglacial system is dominated by aerobic/ anaerobic bacteria and probably viruses in basal bedrock and subglacial lakes. It also contains diverse, metabolically active archaeal, bacterial and fungal species [38]; although eukaryotes

As there is no sunlight, chemoautotrophic or chemolithotrophic bacteria obtain energy from inorganic compounds. The inorganic processes associated with chemoautotrophs and chemolithotrophs may make these bacteria one of the most important sources of weathering and

Glaciers are highly sensitive indicators of past and present climate change. Their current area and volume are a response to changes in both temperature and precipitation [13], as glaciers respond to slight but prolonged changes in climate. The study of glacier fluctuations is rel-

Most glaciers are currently retreating. According to the National Snow and Ice Data Center (NSIDC), the total glacier loss per year since 1994 is approximate 400 billion tons [40–46]. The retreat of glaciers is particularly concerning, since it represents hazards for human communities living near them such as outburst floods, landslides, debris flows, and debris avalanches. Additionally, glaciers contribute substantially to water resources, which can be substantially

Global warming is having a great impact on glaciers, because of the change in air temperature and precipitation [48, 49]. Glacier retreat directly affects various atmospheric, climatic, and ecological phenomena. In retreat glaciers, the thickness of ice and snow decreases, and fossil ice emerges, forefield surface increases (**Figure 4**), new soil develops; and they are colonized

evant to provide an understanding of climate change over temporal scales [13].

have not been detected in all subglacial environments examined [5].

gens could be active [2].

110 Glacier Evolution in a Changing World

**4.3. The subglacial ecosystem**

erosion of rocks on Earth [39].

reduced in many areas of the world [47].

**6. Microorganisms in retreat glaciers**

by new prokaryotic and eukaryotic microbial species.

**5. Glacier retreat**

**Figure 4.** Retreat glacier. (A) In retreat glaciers, the thickness of ice and snow decreases, and it is colonized by new species. (B) Rock with lichens. (C) Microorganisms in the newly formed lake. (D) A rock showing the layer of endolithic phototrophic green algae.

The consequences of climate change are different according to the type of glacier. Depending on the location of the glaciers, these can be classified as terrestrial and marine (**Figure 2**). From the terrestrial glaciers, new lakes and rivers are shaped by runoff waters. On the contrary, some glaciers have a marine margin and terminate in a calving front. In glaciers ending on land, there is continuous permafrost at ice front, while calving glaciers present partly or completely temperate tidewater tongues [4].

One of the effects of climate change on glaciers is that the glacial ice melts and disappears, and microbial communities inhabiting them are being seriously affected [50]. Global warming is changing the basal temperature of the ice, going from cold to polythermal, which causes the growth of new microorganisms that are not psychrophiles but mesophiles thus leading to changes in the diversity and composition of microbial populations [51, 52].

The microorganisms that inhabit glaciers can also contribute to the production of heat as a consequence of their metabolic activity [53]. The amount of heat produced in cryoconite holes of glacial surface has been quantified and reaches 10% of the heat that melts the cryoconite walls during the summer [54]. Although these works have been much questioned [22], a recent work by Hollesen et al. [55] has shown that bioheat can accelerate ice melting on glacier surfaces.

Microorganisms play a main role in glaciers, mainly carrying out key processes in the development of soil, biogeochemical cycling and facilitating plant colonization when glaciers have ultimately retired.

#### **6.1. Development of soil**

Global climate change has accelerated glacial retreat. When the glacier ice melts and disappears, recently deglaciated soils establish a new ecosystem at the glacier forefield. Microorganisms are the initial colonizers of these recently exposed soils [7]. Thanks to their metabolic activity, new molecules are obtained that act as nutrients [7]. The microbial community of the newly formed soil is composed of heterotrophic microorganisms, autotrophic microorganisms, and nitrogen-fixing diazotrophs. Allochthonous material is derived from the glacier surface [21, 56], precipitation and aerial deposition [57] and biological sources such as mammal and bird droppings [58]. Additionally, adjacent ecosystems such as marine and subglacial environments are likely to contribute to the nutrient dynamics [58–60].

Downstream of the glacier, torrents are formed from the runoff water. These watercourses carry mineral salts and organic matter that allow the growth of new microorganisms. Biofilms grow on the banks of the streams, containing new microbial communities that although may remain psychrophilic, begin to have majority of psycrotrophic or mesophilic microorganisms.

Endolithic phototrophs, especially green algae and cyanobacteria, grow inside rocks, inhabiting porous rocks near the glacier surface [24]. Rocks are heated by the sun, and water from snow melt can be absorbed, supplying moisture needed for the growth of microorganisms. In addition to being free-living phototrophs, green algae and cyanobacteria coexist with fungi in endolithic lichen communities. Metabolism and growth of these internal rock communities slowly weathers the rock, allowing gaps to develop where water can enter, freeze, and thaw, and eventually crack the rock, producing new habitats for microbial colonization. The decomposing rock also forms a crude soil that can support the development of plant and animal communities in environments where conditions (temperature, moisture, and so on) allow [24].

The ice from the glaciers draws till, forming moraines around and inside the glacier. But it also draws organic matter from bird droppings and from dead plants and animals. In the development of soil, microorganisms break down this organic matter and produce carbon dioxide, water, and heat. Bacteria are responsible for a very little amount of the heat generation in ice, using a broad range of enzymes to chemically break down a variety of organic materials. Many bacteria are motile and can move into the ice channels of permafrost. When conditions become unfavorable, some bacteria survive by forming endospores, which are highly resistant to the cold and the lack of water and food sources. Microbial eukaryotes such as fungi are important because they break down debris, enabling bacteria to continue the decomposition process. They spread and grow by producing many cells and filaments. They can attack organic residues that are too dry or low in nitrogen for bacterial decomposition. Molds are strict aerobes that grow both as unseen filaments and as black, gray, or white fuzzy colonies on the surface. Most fungi are saprophytes; they live on dead material and obtain energy by breaking down organic matter. At last, protists obtain their food from organic matter in the same way as bacteria do but also act as secondary consumers ingesting bacteria and fungi.

### **6.2. Plant colonization**

Microorganisms play a main role in glaciers, mainly carrying out key processes in the development of soil, biogeochemical cycling and facilitating plant colonization when glaciers have

Global climate change has accelerated glacial retreat. When the glacier ice melts and disappears, recently deglaciated soils establish a new ecosystem at the glacier forefield. Microorganisms are the initial colonizers of these recently exposed soils [7]. Thanks to their metabolic activity, new molecules are obtained that act as nutrients [7]. The microbial community of the newly formed soil is composed of heterotrophic microorganisms, autotrophic microorganisms, and nitrogen-fixing diazotrophs. Allochthonous material is derived from the glacier surface [21, 56], precipitation and aerial deposition [57] and biological sources such as mammal and bird droppings [58]. Additionally, adjacent ecosystems such as marine and subglacial environ-

Downstream of the glacier, torrents are formed from the runoff water. These watercourses carry mineral salts and organic matter that allow the growth of new microorganisms. Biofilms grow on the banks of the streams, containing new microbial communities that although may remain psychrophilic, begin to have majority of psycrotrophic or mesophilic microorganisms.

Endolithic phototrophs, especially green algae and cyanobacteria, grow inside rocks, inhabiting porous rocks near the glacier surface [24]. Rocks are heated by the sun, and water from snow melt can be absorbed, supplying moisture needed for the growth of microorganisms. In addition to being free-living phototrophs, green algae and cyanobacteria coexist with fungi in endolithic lichen communities. Metabolism and growth of these internal rock communities slowly weathers the rock, allowing gaps to develop where water can enter, freeze, and thaw, and eventually crack the rock, producing new habitats for microbial colonization. The decomposing rock also forms a crude soil that can support the development of plant and animal communities in environments where conditions (temperature, moisture, and so on) allow [24].

The ice from the glaciers draws till, forming moraines around and inside the glacier. But it also draws organic matter from bird droppings and from dead plants and animals. In the development of soil, microorganisms break down this organic matter and produce carbon dioxide, water, and heat. Bacteria are responsible for a very little amount of the heat generation in ice, using a broad range of enzymes to chemically break down a variety of organic materials. Many bacteria are motile and can move into the ice channels of permafrost. When conditions become unfavorable, some bacteria survive by forming endospores, which are highly resistant to the cold and the lack of water and food sources. Microbial eukaryotes such as fungi are important because they break down debris, enabling bacteria to continue the decomposition process. They spread and grow by producing many cells and filaments. They can attack organic residues that are too dry or low in nitrogen for bacterial decomposition. Molds are strict aerobes that grow both as unseen filaments and as black, gray, or white fuzzy colonies on the surface. Most fungi are saprophytes; they live on dead material and obtain energy by breaking down organic matter. At last, protists obtain their food from organic matter in the same way as bacteria do but also act as secondary consumers ingesting bacteria and fungi.

ments are likely to contribute to the nutrient dynamics [58–60].

ultimately retired.

**6.1. Development of soil**

112 Glacier Evolution in a Changing World

Retreating glacier fronts expose large expanses of deglaciated forefield, which become colonized by microbes and plants. The space that had been occupied by a glacier which only contained psychrophilic microorganisms is occupied primarily by mesophilic microorganisms inside and on the ice. When this ice disappears and soil begins to develop, rocks and tilt emerge in the moraines; this soil is colonized by lichens on rocks, by algae in streams and by higher plants and animals on the forefield. Most green algae inhabit freshwater, while others are found in moist soil [24]. Other green algae live as symbionts in lichens growing on rocks. In the newly formed soil, mainly consisting of permafrost, the growth of small plants begins. Their roots fragment the ground, forming small channels through which the water that carries ions in solution runs. In this way, the permafrost is fragmented, and it freezes less and less.

In glacier forelands, soil microorganisms are essential for plant growth as they play a key role in the nutrient cycling. In this phase, nitrogen, phosphorus, and other nutrients accumulate and facilitate succeeding plant growth [61]. Nitrogen-fixing plants are common in the primary succession of newly deglaciated soils [62]. Such plant-driven changes to soil nitrogen cycling have significant effects on the establishment of subsequent plant communities [63]. Rhizosphere microbial communities are fundamental for soil cycling, and they are mainly dominated by Proteobacteria, Bacteroidetes, Acidobacteria, Actinobacteria [64], and Firmicutes [65].

#### **6.3. Biogeochemical cycling**

Given their coverage at a global scale, snow and ice could have a major and underestimated role in global biogeochemical cycling [14]. It is essential to know how climate change is shaping the distribution and diversity of microbial communities, since microorganisms are very important components in several biogeochemical processes [66] and in food webs [67].

Nutrient matter in retreat glaciers is variable. The carbon content in forefields is very little. It comes from three distinct sources: autochthonous primary production by autotrophic microorganisms; the deposition of allochthonous material; and ancient organic pools derived from under the glacier [7]. Carbon dioxide is removed from the atmosphere primarily by photosynthesis of snow algae and cyanobacteria, and marine microorganisms in marine glaciers; and it is returned to the atmosphere by chemoorganotrophic microorganisms. Glaciers also provide organic matter to downstream ecosystems [7].

Other important nutrients in forefield soils such as nitrogen in the forms of nitrate, nitrite, and ammonia are microbially fixed from atmospheric nitrogen by cyanobacteria and some other bacteria. There are also external sources such as snowmelt, aerial deposition, and the breakdown of complex organic material or sedimentary bedrocks [7]. Bioavailable phosphorus and iron are usually abundant in the topsoil or bedrock of glaciated regions from weathering of the mineral surface [5].

#### **6.4. Acidification or alkalinization of runoff waters**

Another important effect of glacier retreat is the modification in the chemical composition of the runoff water of the glaciers. When a part of the terrain that had been covered by the glacier is open to the elements, rocks appear on the surface, whose minerals dissolve and change the physical and chemical characteristics of the runoff water. Occasionally, the waters become even toxic because of the presence of heavy metals [68]. Sometimes the formation of alkaline lakes can be observed, due to the mineral salts entrained by the water of runoff in the ground that had been occupied by a glacier, like the Amarga Lagoon in Chile (**Figure 5(A)**). These lagoons can be inhabited by cyanobacteria which grow forming laminar colonies whose calcareous skeletons fossilize generating sedimentary rocks named stromatolites (**Figure 5(B)**). They are formed when cells build up a carbonate skeleton, integrating particles present in the lake water.

Otherwise, when certain minerals such as pirite are exposed to air and water, a slow chemical reaction with molecular oxygen occurs. While this abiotic reaction can lead to the development of acidic conditions, the degree to which acid mineral drainage becomes an overwhelming burden on the environment results from the oxidative dissolution, a reaction catalyzed by microorganisms [69]. This process affects differently to the terrestrial and marine glaciers. In land glaciers, the runoff waters become more acidic, which affects the rivers and lakes that receive their waters. This can affect the flora and fauna, the crops and the human populations that live downstream. When this fact affects the marine glaciers, the composition of marine tidewater tongues changes their chemical composition: water salinity decreases, and at the same time, water becomes more acidic. Acidification of sea water impacts ocean species to varying degrees. A more acidic environment has a dramatic effect on some calcifying species, including oysters, clams, sea urchins, corals, and calcareous plankton [70].

**Figure 5.** Alkalinization of runoff waters. (A) Formation of an alkaline lake (pH 9.1) due to the mineral salts entrained by the water of runoff in the ground that had been occupied by a glacier. The inset shows the location of **Figure 5(B)**. (B) Calcareous skeleton of a stromatolite of Amarga Lagoon at Chile.
