Complex Structure but Simple Function in Microbial Mats from Antarctic Lakes
Microbial mats growing under the permanent ice cover of Antarctic lakes occupy an exceptionally low-disturbance regime. Constant temperature, the absence of bioturbation or physical disturbance from wind action or ice formation allow mats to accumulate, as annual growth layers, over many decades or even centuries. In so doing they often assume decimetre scale, three-dimensional morphologies such as elaborate pinnacle structures and conical mounds. Here we combine existing and new information to describe microbial structures in three Antarctic lakes—simple prostrate mats in Lake Hoare, emergent cones in Lake Untersee and elaborate pinnacles in Lake Vanda. We attempt to determine whether structures emerge simply from uncoordinated organism-environment interactions or whether they represent an example of “emergent complexity”, within which some degree of self-organisation occurs to confer a holistic functional advantage to component organisms. While some holistic advantages were evident from the structures—the increase in surface area allows greater biomass and overall productivity and nutrient exchange with overlying water—the structures could also be understood in terms of potential interactions between individuals, their orientation and their environment. The data lack strong evidence of coordinated behaviour directed towards holistic advantages to the structure, though hints of coordinated behaviour are present as non-random distributions of structural elements. The great size of microbial structures in Antarctic lakes, and their relatively simple community composition, makes them excellent models for more focused research on microbial cooperation.
KeywordsBiofilm Stromatolite Self-organising structures Microbial structures Microbial ecology
The information presented in this contribution is derived from field and laboratory work that would have been impossible without the support of many people and organisations. Logistic support was provided by Antarctica New Zealand, the US Antarctic Program and Antarctic Logistics Centre International. We thank all of our Antarctic field colleagues, in particular Drs Dale Andersen and Tyler Mackey, without whom the underwater research would not have been possible. We also thank the reviewers and editors for helpful comments and hard work to see the volume to production.
Compliance with Ethical Standards
This study was funded by NASA Astrobiology: Exobiology and Evolutionary Biology (NNX08AO19G and NN13AE77A), the New Zealand Ministry of Business Innovation and Employment (CO1605 and UOWX1401), the National Science Foundation (MCM-LTER grant number 1115245) and the Tawani Foundation.
Conflict of Interest
Ian Hawes declares that he has no conflict of interest. Dawn Sumner declares that she has no conflict of interest. Anne D. Jungblut declares that she has no conflict of interest.
This article does not contain any studies with human participants or animals performed by any of the authors.
- Dana GL, Wharton RR, Dubayah R (1998) Solar radiation in the McMurdo Dry Valleys, Antarctica. In: Priscu JC (ed) Ecosystem dynamics in a polar desert: The McMurdo Dry Valleys, Antarctica. American Geophysical Union, Washington, DC, pp 38–64Google Scholar
- De Wolf T, Holvoet T (2005) Emergence versus self-organisation: different concepts but promising when combined. In: Brueckner S, Di Marzo Serugendo G, Karegeoros A, Nagpal R (eds) Engineering self organising systems: methodologies and applications. lecture notes in computer science. Springer, Berlin, pp 1–15Google Scholar
- Haendel D, Kaup E, Loopman A, Wand U (1995) Physical and hydrochemical properties of water bodies. In: Bormann O, Fritzsche D (eds) The Schirmacher Oasis, Queen Maud Land, East Antarctica, and its surroundings. PGM Ergh 289. Perthes, Gotha, pp 259–319Google Scholar
- Howard-Williams C, Schwarz A-M, Hawes I (1998) Optical properties of the McMurdo Dry Valley Lakes, Antarctica. In: Priscu JC (ed) Ecosystem dynamics in a Polar Desert: the McMurdo Dry Valleys, Antarctica. American Geophysical Union, Washington, DC, pp 189–205Google Scholar
- Kaup E, Loopman A, Klokov V, Simonov I, Haendel D (1988) Limnological investigations in the Untersee Oasis during the summer season 1983/84. In: Martin J (ed) Limnological studies in Queen Maud Land. Academy of Sciences, Tallinn, Estonia, pp 43–56Google Scholar
- Petroff AP, Beukes NJ, Rothamn DH, Bosak T (2013) Biofilm growth and fossil form. Phys Rev. https://doi.org/10.1103/PhysRevX.3.041012
- Reyes K, Gonzalez NI, Stewart J, Ospino F, Nguyen D, Cho DT, Ghahremani N, Spear JR, Johnson HA (2013) Surface orientation affects the direction of cone growth by Leptolyngbya sp. strain C1, a likely architect of coniform structures Octopus Spring (Yellowstone National Park). Appl Environ Microbiol 79:1302–1308CrossRefGoogle Scholar
- Seckbach J, Oren A (2010) Microbial mats: modern and ancient microorganisms in stratified systems. Cellular origin, life in extreme habitats and Astrobiology 14. SpringerGoogle Scholar
- Spigel RH, Priscu JC (1998) Physical limnology of the mcmurdo dry valley lakes. In: Priscu JC (ed) Ecosystem dynamics in a Polar desert: the mcmurdo dry valleys, Antarctica. AGU, Washington, DC, pp 153–189Google Scholar
- Stahl LJ, Bolhuis H, Cretoiu MM (2018) Phototrophic marine benthic microbiomes: the ecophysiology of these biological entities. Environ Microbiol. https://doi.org/10.1111/1462-2920.1449
- Vincent WF (2000) Cyanobacterial dominance in polar regions. In: Whitton BD, Potts M (eds) The ecology of cyanobacteria. Kluwer Academic Publishers, Dordrecht, pp 321–340Google Scholar
- Wharton RA Jr, McKay CP, Clow GD, Andersen DT (1993) Perennial ice covers and their influence on Antarctic lake ecosystems. In: Green WJ, Friedmann EI (eds) Physical and biogeochemical processes in Antarctic lakes. Antarctic research series. American Geophysical Union, Washington, DC, pp 53–70CrossRefGoogle Scholar