Introduced/Indigenous/Endemic Microorganisms

One of the major considerations that face microbiologists and mycologists studying Antarctic microorganisms is determining whether these organisms are indigenous, endemic or introduced to Antarctica. Antarctic microbial ecosystems provide useful models for general questions in evolutionary ecology, given the relative isolation of the region, the severe biological constraints imposed by the harsh environment, and the absence of higher plants and animals. Endemic organisms are defined as organisms that are only found in the place of interest, while indigenous is defined as originating from the place of interest, or present at the time of first human occupation, as opposed to exotic or introduced which are defined as bought into the place of interest by humans, or that have self introduced since the first human occupation. Areas such as Lake Vostok, located in the heart of Antarctica (78.5ºS, 106.8ºE), under the East Antarctic ice sheet, is a sealed environment due to the thick layer of ice that has accumulated over the top of the lake which has prevented introduction of new material. This lake provides a unique, natural culture collection of endemic microorganisms that have been isolated from the global gene pool over timescales (over 400,000 years) of evolutionary significance (Abyzov, 1993). Lake Vostak’s ice sheet is providing insight into the introduction and evolution of microorganisms into the Antarctic environment and has acted as a collection depot for airborne propagules for over

400,000 years. Microbiological studies of cores drilled through the ice from 4.5 km above sea level to 1 km below sea level showed the presence of viable species including some unique to Antarctica (Abyzov, 1993). The diversity of organisms throughout the core has varied over time, indicating different introductions at different periods.

Most Antarctic environments, unlike Lake Vostok, however continue to receive microbial propagules from outside the Antarctic region as indicated by spore trap data of the air (Marshall, 1997), the microflora found in Antarctic snow and ice, the colonising taxa at geothermal sites on Mount Erebus, and the high frequency of apparently cosmopolitan species in most habitats (Kerry, 1990b; Azmi and Seppelt, 1998). Differences in environmental stability and selection pressure among environments are likely to influence the degree of adaptive radiation and microbial endemism. If microbial endemism (genotypes of microorganisms specific to geographical region (Vincent, 2000)) is possible, then Antarctica is one of the most likely regions for such organisms because of the isolated and extreme nature of the environment, reduced human influence, lack of transport into and around Antarctica, and few animals. The Antarctic environment is therefore an ideal ecosystem to examine the evolutionary processes that can give rise to microbial speciation.

There is evidence of endemic species in highly specialised niches on the continent such as the endolithic habitats and lake biomats in the McMurdo Dry Valleys of Antarctica. Selbmann et al. (2005) reported on the isolation of black, meristematic fungi, Friedmanniomyces sp. and Cryomyces sp., from cryptoendolithic lichen-dominated communities in Antarctic rock samples collected from Linnaeus

Terrace, McMurdo Dry Valleys. Thelebolus globosus Brumm. & de Hoog and Thelebolus ellipsoideus Brumm. & de Hoog are newly described fungi from the biomats of the McMurdo Dry Valleys and both are endemic to Antarctica according to de Hoog et al. (2005).

According to Vishniac (1996), to characterise a species as indigenous requires one or more of the following:

• the presentation of evidence of visible growth in situ.

• unique occurrence of the species with adaptation to the environmental conditions.

• occurrence of adapted species in excess of probable immigration numbers.

Uydess and Vishniac (1976) demonstrated in situ growth of bacteria in McMurdo Dry Valley soils indicating that some of the viable forms are indigenous. Vishniac and Hempling (1979) came to the same conclusion using the growth of the Antarctic yeast Cryptococcus spp., Sporobolomyces spp. and Tilletiopsis spp..

Atlas et al. (1978) reported that high levels of yeast isolated from Antarctica soils were due to the yeasts increased ability to survive after spore deposition from the air. Atlas et al. (1978) also stated the yeasts have an psychrophilic-psychrotrophic nature, which assists them to withstand the cold desiccation conditions of Antarctica as well as to grow during the diurnal freeze thaw cycles at the soil surface during the Antarctic summer. Their studies which involved sampling soils from 44 areas including the Dry Valleys and Tran Antarctic Mountains concluded that yeasts were more abundant in coastal soils where moisture contents were higher and in areas of high human impact and plant growth.

The invasion process for Antarctic microbes are more varied than for larger biota and includes atmospheric circulation, and vectoring by birds, fish, marine mammals and humans. Once established within the Antarctica environment, microorganisms can be redistributed by these same vectors. Arguably mosses may be the closest to microbes for introductions, Skotnicki et al. (1998) reported the finding of a single colony of Bryum pseudotriquetrum near Lake Fryxell that was identical to shoots from another turf some 40 km away at Cape Chocolate, indicating that mosses can be dispersed by the strong winds prevalent in the region, and that when environmental conditions are favourable enough for growth to occur, it is possible for moss propagules to colonise new areas. Spore trapping by Marshall (1997) on Signy Island showed that high concentrations of viable, locally derived propagules from plants infected with fungi were present as the Island is partially covered in vegetation.

Surprisingly, the volcanic areas of Antarctica contain very similar diversity of microorganisms as other volcanic areas around the world (Broady et al., 1987). In evolutionary biology, convergent evolution describes the process whereby organisms not closely related independently evolve similar traits as they both adapt to similar environments (Waterman, 1999). This similarity may be due to the unique soil and environmental conditions associated with volcanic environments such as low nitrogen and phosphorus levels, high levels of potentially toxic chemicals, high pH, and consistent temperature (Bargagli et al., 2004). Local cold propagules may find it to difficult to colonise this soil type due to the unique soil and environmental conditions.

The migratory nature of Antarctic birds, fish and mammals make them ideal vectors to introduce foreign microorganisms into Antarctica. Geomyces pannorum was shown to be dispersed around Signy Island on skua feathers (both on the skua and in molten feathers) and seal skins (Marshall, 1998). McRae et al. (1999) sampled Antarctic bird nests at Windmill Islands, and concluded that Penicillium sp. were more commonly isolated from areas inhabited by birds rather than areas where plants were present. They offered two explanations, one the increase in nutrients enhanced soil inhabiting Penicillium sp. growth or that Penicillium sp.

were transported to Antarctica on the body and feathers of the birds. Siegfried (1981) estimated that bird materials contributed 0.4 tonnes (dry weight) ha ^-1 year

-1 onto coastal lowlands. In areas of bird nesting this is estimated to be a lot more.

Melick and Seppelt (1994) estimated that mosses and lichens contributed 2.4mg grm^-1sugars to the soil.

Climatic constraints and geological isolation are largely responsible for the present day low biodiversity and structural simplicity of the Antarctica ecosystem (Kennedy, 1995). Global warming has been suggested to be assisting in the survival of microorganisms in the Antarctic climate (Frenot et al., 2005) and may also affect biodiversity in the future. The long term effects of global warming include reduction of the ice cover, leading to increased rock weathering, increased egression of water, melting of permafrost and increased soil activity. Antarctica is known for decreasing biodiversity the further south the latitude. As global warming takes affect, it is expected that species which are at present not found at the southern latitudes will begin to inhabit these latitudes. Many plants are constrained by the Antarctic environment and display dwarf, cushions and prostate growth forms but with global warming it is expected that they will take

on tall faliose, canopy and hummock-forming habits. As the temperature warms, if global warming is verified in the future, there will be many changes to the ecosystem functioning both negative and positive, plants will increase productivity but the nutrient limited soils of Antarctica will limit production.

There will be an increase in decomposition rate due to increased microbial activity with the warmer climate to offset the nutrient limits but this will be affected by water levels and possible waterlogging of the soil could lead to reduced decomposition rates (Kennedy, 1995).

Global warming is in part a consequence of a reduction in the ozone layer in the atmosphere; ozone is the major component that adsorbs ultraviolet (UV). UV is known to be adsorbed by deoxyribonucleic acid (DNA), ribonucleic acid (RNA) and proteins and causes fatal damage to cells. Therefore it can be hypothesised that organisms which have the ability to prevent or repair UV damage will dominate the Antarctic ecosystems. An increase in atmospheric carbon dioxide (CO2) is a consequence of global warming, increased CO2 increases plant productivity but there must be other resources available to sustain long term increased productivity. Atmospheric green house gases concentration will not only affect the surface temperature but they will also affects the amount of precipitation. Cold air is not able to hold as much moisture as warm air so as the air warms the amount of water vapour in the air will increase. In Antarctica, it is expected that the water availability will increase leading to increasingly complex communities developing, changes in the ecosystem functioning and generally increased biological activity.

There are a large variety of cosmopolitan species being isolated and identified from habitats within Antarctica which also suggests airborne introduction. There is a growing pool of evidence that micoorganisms are arriving in Antarctica by atmospheric circulation. Much of the evidence is from the Antarctic Peninsula where pollen from South American plants has been found and spore trapping detected intermittent arrival of spores from other regions when wind conditions were appropriate (Marshall, 1997). Another indicator of atmospheric invasion is the biodiversity in the ice shelves, spores and cells from species of microbiota that have not been found as living cells within Antarctic ecosystems have been found trapped in layers in the ice shelf .

An increasing human presence in Antarctica has accelerated the potential arrival of foreign microoroganisms. The building of bases, increased logistics, importation of supplies, and disposal of rubbish increased the chances of introduction of new organisms. This includes the potential introduction of infectious diseases which can affect Antarctic mammals and birds. Once a microbial propagule arrives at a potential habitat in Antarctica, the environment is likely to exert a strong selection pressure. As Antarctica is open to such invasion from other regions, it is natural that microbiota will evolve within the environment to become new endemic species or via gene transfer to displace the already endemic organisms (Vincent, 2000). Two different views exist on the likelihood of endemic organisms. One is that everything is everywhere and that environmental conditions select what survives and proliferates; this view implicates that endemic organisms are rare (Staley and Gosink, 1999). The counter view is that the Antarctic region is more isolated than other parts of the world, that it is aerobiology differs from elsewhere, that local dispersal processes

favouring local species are more efficient than long range dispersal and that there has been environmental selection for specific adaptive strategies over a period of several million years leading to endemic Antarctic organisms (Vincent, 2000).

Very little is known about either the levels of endemicity in the various microbial groups present in Antarctica or the presence or population trends of alien species.

It was within the cryptoendolithic microbial communities, that the first endemic Antarctic fungal species Friedmanniomyces endolithicus anam.-gen. and Friedmanniomyces endolithicus sp. nov. were isolated (Onofri et al., 2000).

Molecular analysis is allowing for more in depth investigation into origins and differences between Antarctic organisms and similar organisms in different regions. The comparison of Antarctic organisms DNA sequences with DNA sequences of other organisms contained in databases is leading to confirmation of the identity of Antarctic organisms and highlighting relativeness between Antarctic species and species from other regions. The more DNA sequences, from a variety of location and regions of the DNA strand analysed increases the accuracy of this type of analysis compared with the analysis of a small part of ribosomal DNA sequences.

Despite Antarctica’s isolation, introduced microbes, fungi, plants and animals occur on most of the sub-Antarctic islands and some parts of the Antarctic continent. These have arrived over approximately the last two centuries, coinciding with human activity in the region. They have both direct and indirect impacts on the functioning of species in the limiting Antarctic ecosystems including substantial loss of local biodiversity and changes to ecosystem processes. Successful biological invasions are amongst the most significant threats

to biodiversity, posing both a significant threat to individual species and being responsible for major changes to ecosystem structure and functioning. Their extent and significance are likely to increase with global environmental change.

Biodiversity is another concern and the dangers of importation of microorganisms into Antarctica and the movement of these organisms between different parts of the continent was recognised (Wynn-Williams, 1996) but there have been few attempts to quantify or minimise the risk or assess the impact on native microbial floras. Azmi and Seppelt (1998) reported a total of 35 taxa of fungi from the Windmill Island of which 12 were restricted to soils in the vicinity of Casey Station suggesting their introduction were associated with human activities. Kerry (1990b) reported 20 taxa from Vestfold Hills and MacRobertson Land of which 10 were most common in sites affected by human activities and their presence was interpreted as a result of human activities. Human microorganisms discharged with raw sewage from Antarctic bases have been located in the surrounding marine environment and sea ice. Lisle et al., (2004) traced the distribution of Clostridium perfringens (an indicator organism for faecal contamination within an environment) from Antarctica’s largest base, U.S. McMurdo station to just beyond 400 m from the base’s sewage outfall noting that the concentration of bacteria decreased with sediment depth and distance from the outfall, but, nonetheless, Clostridium perfringens, was also found in the intestines of marine animals within the 400 m zone.