PerspectiveMicrobiology

No Place Too Cold

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Science  19 Jun 2009:
Vol. 324, Issue 5934, pp. 1521-1522
DOI: 10.1126/science.1173645

Even the coldest environments on Earth have enough liquid water to sustain life. The scope for biological productivity in the polar regions is constrained by low temperatures and low annual levels of solar radiation, but free water on or under glaciers or ice sheets nevertheless contains numerous species of mostly microorganisms. These delicate ecosystems are widely regarded as sentinels of climate change. Recent studies of polar and glacial lakes, as well as subglacial environments, have shed light on how these ecosystems function and on the role that they play in nutrient cycling.

Typical microbial food web structure in the plankton of an Antarctic lake.

There are few or no multicellular organisms. The truncated, simple food web is dominated by viruses, bacteria, algae, and protozoans. Dissolved organic carbon includes photosynthate exuded by phytoplankton, used as an energy source by bacteria. Most viruses appear to infect bacteria in these lakes.

CREDIT: P. HUEY/SCIENCE

The Antarctic is an isolated, largely ice-covered continent with little scope for colonization. Here, bacteria, algae, and flagellated and ciliated protozoans are abundant in the numerous lakes and in free water on and under glaciers, where they form simple truncated food webs. The penguins and seals on Antarctica's margins are not part of this terrestrial biota, but are instead members of the highly productive marine ecosystem. In contrast to Antarctica, the Arctic is an extension of continental land masses such as North America and Asia. Moreover, the climate is generally less severe than in Antarctica. The Arctic therefore has higher plants, land mammals, and birds, and microorganisms are more abundant in the lakes, on glaciers, and in the often well-developed soils. Glaciers at all latitudes represent extreme environments and are always dominated by microorganisms.

The most detailed knowledge of polar ecosystems comes from studies of Antarctic lakes, situated in the small areas of the continent that are ice-free. The lakes contain simple, truncated food webs dominated by microorganisms (see the figure). Cryptophytes are among the most ubiquitous photosynthetic flagellates found in polar lakes. They are microscopic plantlike organisms adapted to low light levels and low temperatures that can feed on bacteria or dissolved organic carbon as well as undertaking photosynthesis (1, 2). This mixed nutrition (mixotrophy) provides photosynthetic flagellates with nutrients for photosynthesis and/or to supplement their carbon budgets. Mixotrophic ciliates (such as Mesodinium rubrum) are also common. In general, nutritional versatility is the key to success: For example, some nonphotosynthetic flagellates, such as Diaphanoeca grandis, take up dissolved organic carbon but also feed on bacteria.

Bacteria in Antarctic lakes function throughout the year under lake ice cover. Even in winter, bacterial growth is measurable, but overall rates are much lower than those in lower-latitude systems. Unique selection pressures in polar environments provide an ideal setting to study endemism. Existing data show that many strains are cosmopolitan, but there is clear evidence for novel bacterial species (3, 4).

Viruses in lakes largely infect bacteria and, by lysing the host cell, recycle carbon to the organic carbon pool before it can be transferred up the food chain by protozoan predation on bacteria. They thus effectively shortcircuit the carbon cycle. In low-latitude lakes, only ∼0.6% to 4.2% of bacteria may be infected by viruses, whereas in some Antarctic lakes, 22% to 34% of bacteria may be parasitized by viruses (5). However, the low rates of bacterial growth in polar waters means that infected bacteria cannot produce many viruses; on average, only 4 viruses are released from a bacterial cell when it is lysed, compared with a mean of 26 viruses across temperate lakes. These high infections rates suggest a significant impact on carbon cycling (5).

In glaciers, biologically mediated processes also seem to play an important role in nutrient cycling (6). Glacier surfaces develop minilakes called cryoconites—near-vertical tubes with a sediment layer at the bottom overlain by water. In Antarctica, cryoconites are entombed by an ice cover, whereas in the Arctic and in lower-latitude glaciers, they are usually open to the air. They freeze up in winter and have liquid water during summer as solar radiation heats the dark sediment.

The communities in cryoconites resemble those of Antarctic lakes (see the figure). In Antarctica, cryoconites contain viruses, bacteria, cyanobacteria, algae, flagellates, and ciliates. In the Arctic and lower-latitude glaciers, they may also contain microscopic animals such as nematodes and rotifers. Comparative studies, including bacterial ribosomal DNA analyses, indicate that cryoconites are colonized by organisms from nearby lakes and streams (7).

Investigations of biogeochemical cycling on glacier surfaces are relatively recent. The evidence from Arctic glaciers suggests that much more organic carbon is deposited from the surrounding environment than is fixed on the glacier during photosynthesis (8). On Arctic glaciers, respiration appears to exceed photosynthesis, indicating that surface glacier ecosystems are subsidized by carbon inputs from the environment, rather like streams and estuaries. Whether this is true of Antarctic glaciers remains to be shown.

Liquid water at the bases of glaciers can also support bacterial communities, including aerobic strains and anaerobic nitrate and sulfate reducers and methanogens (9). For example, Blood Falls—an iron-rich discharge emanating from the Taylor Glacier in Antarctica—derives from a brine pocket trapped in the glacier 1.5 million years ago. This brine contains a microbial community that mediates a sulfur cycle in which Fe(III) is the terminal electron acceptor; Fe(III) may be an important electron acceptor for many subglacial ecosystems (10).

A network of subglacial lakes under the Antarctic ice cap have yet to be sampled. They have been isolated for millions of years, but a molecular analysis of accretion ice above Lake Vostok revealed a bacterial community with species typical of aquatic environments. If these species are characteristic of the underlying lake, this would indicate that it does not possess an evolutionary distinct biota (11).

As investigations of polar microbial biodiversity forge ahead, key challenges will be to unravel the roles of different groups in ecosystems and to identify the biochemical mechanisms, such as cold-adapted proteins, that enable survival in extreme environments. Advances in functional genomics and proteomics will provide exciting insights into how life evolved and functions under extreme conditions.

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