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Rapid Microbial Response to the Presence of an Ancient Relic in the Antarctic Dry Valleys

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Rapid Microbial Response to the Presence of an Ancient Relic in the Antarctic Dry Valleys ARTICLE Received 16 Aug 2011 | Accepted 14 Dec 2011 | Published 7 Feb 2012 DOI: 10.1038/ncomms1645 Rapid microbial response to the presence of an ancient relic in the Antarctic Dry Valleys Grace Tiao1,2, Charles K. Lee1, Ian R. McDonald1, Donald A. Cowan3 & S. Craig Cary1,4 The extreme cold and aridity of the Antarctic McMurdo Dry Valleys have led to the longstanding belief that metabolic rates of soil microbiota are negligible, and that ecosystem changes take place over millennia. Here we report the first direct experimental evidence that soil microbial communities undergo rapid and lasting changes in response to contemporary environmental conditions. Mummified seals, curious natural artifacts found scattered throughout Dry Valleys, alter their underlying soil environment by stabilizing temperatures, elevating relative humidity and reducing ultraviolet exposure. In a unique, multi-year mummified seal transplantation experiment, we found that endemic Dry Valley microbial communities responded to these changes within 3 years, resulting in a sevenfold increase in CO2 flux and a significant reduction in biodiversity. These findings challenge prevailing ideas about Antarctic Dry Valley ecosystems and indicate that current and future environmental conditions may strongly influence the ecology of the dominant biota in the Dry Valleys. 1 The International Centre for Terrestrial Antarctic Research, Department of Biological Sciences, University of Waikato, Private Bag 3105, Hamilton 3240, New Zealand. 2 Merton College, Oxford OX1 4JD, UK. 3 Institute for Microbial Biotechnology and Metagenomics, University of the Western Cape, Cape Town 7535, South Africa. 4 College of Earth, Ocean, and Environment, University of Delaware, 700 Pilottown Road, Lewes, Delaware 19958, USA. Correspondence and requests for materials should be addressed to S.C.C. (email: [email protected]). NATURE COMMUNICATIONS | 3:660 | DOI: 10.1038/ncomms1645 | www.nature.com/naturecommunications © 2012 Macmillan Publishers Limited. All rights reserved. ARTICLE NatUre cOMMUNicatiONS | DOI: 10.1038/ncomms1645 ince Scott’s 1901–1904 Discovery expedition, mummified seals have been reported in the McMurdo Dry Valleys of Antarctica Sin locations up to 66 km inland and 1,800 m above sea level1–7. These curious, twisted remnants of bone and desiccated flesh (Fig. 1a) are many hundreds of years old, preserved by extremely cold and arid conditions1,2,5,6. Why they journey over such challeng- ing terrain to arrive at these remote resting places is unknown and has generated much speculation2,4,5, and theories have ranged from the random dispersal of disoriented pups during prolonged bad weather2 to outbreaks of phocine distemper virus6. Meanwhile, the ecological significance of the phenomenon has remained unexplored. The Dry Valleys comprise one of the most inhospitable, trophi- cally simple ecosystems on Earth8,9. Devoid of vascular plant life8–10, the Dry Valley ecosystem supports only a handful of microscopic invertebrate, lichen and moss species9,10. However, the bulk of Dry Valley biodiversity and biomass consists of edaphic bacteria8,11,12, as few other organisms can endure the region’s extreme tempera- ture and light regimes, high soil salt concentrations, near-negligible levels of organic C and N, and scarcity of liquid water10,12. It has been suggested that these soil microbial communities are princi- pally sustained and structured by the location and distribution of legacy C sources in the form of ancient lake sediments13–16. Under this hypothesis, contemporary environmental conditions exert lim- ited influence on community dynamics13,15, as microbial activity in the Dry Valleys has, until recently, been thought to be exceptionally low compared with temperate ecosystems13,15. Activity is further restricted to brief periods during austral summers, when liquid water may be available in certain niche habitats17–19. As a result, changes in soil ecology are believed to take place over centuries and even millennia13,15, despite the fact that no direct stud- ies have been conducted on rates of change in microbial community structure and function. Instead, researchers studying Dry Valley soil ecosystems have used CO2 efflux and rates of organic C turnover in soil as proxies for microbial activity, and as low activity rates ipso facto preclude changes in community structure, data show- ing low rates have been taken to indicate slow rates of change in microbial communities. For example, Johnston and Vestal’s study of Dry Valley cryptoendoliths20 used the slow lipid C turnover rate (~20,000 years) to support the claim that they are the slowest- growing communities on earth. Therefore, despite widespread Figure 1 | Mummified seal carcasses in the Miers Valley. (a) A seal acknowledgment of the susceptibility of Dry Valley microbial com- carcass in a stage of advanced mummification. (b) The mummified seal munities to seasonal variations in biological activity15,21–23, no study carcass used for the seal movement experiment. has described or predicted rapid and sustained changes in commu- nity structures caused by contemporary environmental conditions. More recent studies have shown that the Dry Valleys support a as indicated by radiocarbon dating data of the tissues from a phylogenetically diverse group of microbes12,24,25, and a handful of number of seals in Miers Valley (including the seal, ‘Seal I’, used these studies have speculated that these communities respond on for the movement experiment; Table 1; Supplementary Methods). much shorter, decadal timescales15,19,21,26. In this study we have Radiocarbon dating of Antarctic marine fauna is complicated by the compared soil beneath a seal carcass found in the Miers Valley, marine reservoir effect, which results from the unusual radiocarbon Victoria Land, Antarctica, with soils from nearby exposed control content of Southern Ocean coastal waters. These waters originate sites to characterize the physicochemical and biological modifica- from deep currents that have travelled for millennia along the 14 tions associated with the mummified seal. We measured the rate seafloor, carrying ancient dissolved atmospheric CO2. The C- at which the observed biological changes occurred in response to depleted CO2 then enters the food chain and leads to significant a direct soil modification experiment: after transplanting a Miers overestimation of radiocarbon age for top-level feeders in the Valley mummified seal to an untouched neighbouring site, we used Southern Ocean2,27. To help correct age estimates for the mummy community DNA fingerprinting and amplicon pyrosequencing over tissue, a tissue sample taken from a seal carcass killed during Scott’s several years to track changes in microbial community composition 1904 expedition and left outside the Cape Evans hut was dated and and structure. Our observations in the soil modification experi- used for calibration (Table 1). Mummified seals in this small set of ment confirm the view that microbial communities can respond samples were estimated to be around 250–790 years old (Table 1), to changes in the environment, offering the first direct evidence and are evidently enduring features of the Dry Valley landscape and of rapid microbial response to contemporary environmental condi- ecosystem. tions in the Dry Valleys. Long-term changes beneath a mummified seal. Physicochemical Results comparison of soil beneath an untouched mummified seal carcass Radiocarbon ages of mummified seals. Mummified seals found in Miers Valley (Fig. 1b) with soil from a nearby exposed control within the McMurdo Dry Valleys seem to range widely in age, site of similar geomorphology revealed substantial modifications. NatUre cOMMUNicatiONS | 3:660 | DOI: 10.1038/ncomms1645 | www.nature.com/naturecommunications © 2012 Macmillan Publishers Limited. All rights reserved. NatUre cOMMUNicatiONS | DOI: 10.1038/ncomms1645 ARTICLE Soil N and organic C levels under the seal were elevated to nearly two-tailed t-test) and adenosine triphosphate (ATP) levels (a proxy 7× and 4× the levels in controls, respectively (Table 2), suggesting for microbial biomass and activity) were higher by a factor of 25 that large quantities of seal organic matter were transferred to the (t = 4.241930, P = 0.0017, n = 6; unpaired two-tailed t-test). soil over time. Analysis of the isotopic N composition of seal tissue and seal-covered soil lends further support to this conclusion: Dry Changes in bacterial diversity beneath a mummified seal. Ultra- Valley materials typically have very low fractions of 15N, whereas deep pyrosequencing ( > 30,000 reads per sample, average length seal tissue and seal-covered soil both yielded high 15N fractions 369.5 bp) of bacterial 16S rRNA gene PCR amplicons revealed a characteristic of Antarctic marine-derived materials (Supplemen- significant shift in microbial community structure and a reduction tary Table S1). Differences in total C levels between seal-covered and unaugmented control soils were highly significant (t = 7.754687, P < 0.0001, n = 4 and 6; unpaired two-tailed t-test). Total N and total a Dec-06Jan-07Feb-07Mar-07Apr-07May-07Jun-07Jul-07Aug-07Sep-07Oct-07Nov-07Dec-07Jan-08 20 organic C levels were likewise significantly different between the two sites (t = 7.808302, P < 0.0001, n = 4 and 6; t = 7.432392, P < 0.0001, 10 n = 4 and 6 for total N and total organic C, respectively; unpaired two-tailed t-test). 0 C) ° The presence of the seal carcass appeared to stabilize consid- ( erably the extreme diurnal temperature
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