 |
Science Highlight
Accurately measuring deep-sea microbial activities and their impacts on biogeochemical cycles
Christian Tamburini1*, Douglas H. Bartlett2, Rita R. Colwell3, Jody W. Deming4, Chiaki Kato5, John W. Patching6 and Carol M. Turley7
1Université de la Méditerranée, Centre d'Océanologie de Marseille, LMGEM, Marseille, France ; 2Scripps Institution of Oceanography, University of California, La Jolla, CA, USA ; 3University of Maryland, Biotechnology Institute, College Park, USA ; 4School of Oceanography, University of Washington, Seattle, USA ; 5JAMSTEC, Yokosuka, JAPAN ; 6 Martin Ryan Institute, National University of Ireland, Galway, IRELAND ; 7Plymouth Marine Laboratory, Plymouth, UK
*corresponding author: christian.tamburini@univmed.fr
The effects of elevated hydrostatic pressure concern all organisms living in the world’s largest (by volume) habitat: the deep sea. Historically underestimated in terms of its contribution to the Biosphere, the deep sea remains one of the least known and most poorly understood environments on our planet. The implementation plan for the joint SOLAS-IMBER ocean carbon research points out the need to study microbial activities under in situ pressure conditions (see p.32) to improve this situation, but states, we believe incorrectly, that deep-sea microbial activity is “commonly” measured at atmospheric pressure with resulting rates “higher than might be expected." From decades of research paying close attention to the use of in situ conditions, we know that life in the deep sea is more complicated than this. The aim of this short article is to summarise knowledge of pressure effects on microbes in the deep sea and redress this mischaracterization.
The field of deep-sea microbiology was born 125 years ago and pressure-adapted microbes or piezophiles (also known as barophiles) have been obtained readily from many different deep-sea regions by researchers around the world. These organisms include members of the domains Archaea and Bacteria. Various archaeal isolates within both the Euryarchaea and Crenarchaea kingdoms have been obtained, along with bacterial strains belonging to the genera Carnobacterium, Colwellia, Desulfovibrio, Marinitoga, Moritella, Photobacterium, Pyschromonas, and Shewanella (reviewed in1). The membrane properties of piezophiles have been well described and the unique abilities of piezophiles to be motile, transport nutrients, and undergo DNA replication and translation under high pressure are being studied2. Protein adaptation to high pressure has also been examined in comparative studies of piezophiles and microbes adapted to atmospheric conditions3.
The first measurements of deep-sea microbial activity made without pressure changes were reported by Jannasch and Wirsen (1973), who concluded that "elevated pressure decreases rates of growth and metabolism of natural microbial populations collected from surface waters as well as from the deep sea"4. Contrary to this early conclusion, virtually all other data from the water column obtained under in situ conditions have shown that the trend is the reverse: microorganisms at depth are adapted to both the high pressure and low temperature conditions of their environment. Hence incubation of deep-sea samples at atmospheric pressure commonly underestimates (not overestimates, as written in the SOLAS-IMBER Implementation Plan) in situ activity under ambient conditions5-8. Exceptions to this general trend occur only under specific conditions; for example, with a large charge of particles or mixing waters9 or according to the substrate used10.
Microbial communities in the deep ocean may contain both autochthonous microbes adapted to in situ temperature and pressure and allochthonous microbes transported from the ocean surface layer, for example by settling particles. Activities of the allochthonous microbes decrease with depth, limiting their capacity to degrade organic matter sinking through the water column11-13. They may be inactive (though not dead) under deep in situ conditions, but can dominate (or form a significant portion of) community activity when measured under surface pressures and/or temperatures. Thus, community activity measurements made under surface versus deep-sea conditions may reflect entirely different components of the community: one cannot predict in situ activity from unpressurised incubations14-16!
Only with microbial rates measured under in situ conditions (e.g., high-pressure, low temperature, ambient food availability) do realistic calculations of the flow of matter and energy as mediated by microbes become possible for the deep sea, and thus throughout the water column. By combining such rate measurements with recent developments on single cell approaches and new insights highlighting possible chemoheterotrophy, we can expect to better understand elemental cycles in the mesopelagic and bathypelagic zones – a welcome key objective within joint SOLAS-IMBER ocean carbon research.
Fig A – Schematic diagram showing the flux of carbon through the NE Atlantic water column to the deep-sea sediment. REPRODUCED FROM Turley, FEMS Microbiol. Ecol., 2000).
Fig B – High Pressure Serial Sampler (HPSS, Bianchi et al., DSR, 1999) fitted on a classical Sea-Bird Carousel to sample deep-sea waters without change of in situ pressure condition (see www.com.univ-mrs.fr/~tamburini).
Fig C – Samples from Mariana Trench Challenger Deep at a depth of 10,898 m on February 28, 1996 (Kato et al., Extremophiles 1997).
1. D. H. Bartlett, F. M. Lauro, E. A. Eloe, in Physiology and biochemistry of extremophiles C. Gerday, N. Glandsdorf, Eds. (American Society for Microbiology Press, Washington, D. C., 2007) pp. 333-348
2. F. M. Lauro et al., Journal of Bacteriology, JB.01176 (December 21, 2007, 2008)
3. C. Kato et al., in Protein Adaptation in Extremophiles. Molecular Anatomy and Physiology of proteins series T. Thomas, K. S. Siddiqui, Eds. (Nova Science Publisher, 2008)
4. H. W. Jannasch, C. O. Wirsen, Science 180, 641 (1973)
5. P. S. Tabor et al., Microbial Ecology 7, 51 (1981)
6. H. W. Jannasch, C. O. Wirsen, Applied and Environmental Microbiology 43, 1116 (1982)
7. J. W. Deming, P. S. Tabor, R. R. Colwell, in Advanced concepts in Ocean measurements for marine biology F. Diemer, J. Vernberg, D. Mirkes, Eds. (University of South Carolina Press, Columbia St, 1980) pp. 285-305
8. C. Tamburini, J. Garcin, A. Bianchi, Aquatic Microbial Ecology 32, 209 (2003)
9. A. Bianchi, J. Garcin, G. Gorsky, M. Poulicek, O. Tholosan, Comptes Rendus de l'Académie des Sciences de Paris 322, 1113 (1999)
10. J. W. Patching, D. Eardly, Deep-Sea Research I 44, 1655 (1997)
11. C. Tamburini et al., Aquatic Microbial Ecology 43, 267 (2006)
12. C. M. Turley, Deep-Sea Research I 40, 2193 (1993)
13. C. M. Turley, K. Lochte, R. S. Lampitt, Phil. Trans. R. Soc. Lond. N 348, 179 (1995)
14. D. F. Eardly, M. W. Carton, J. M. Gallagher, J. W. Patching, Progress in Oceanography 50, 249 (2001)
15. J. W. Deming, in ASM Manual of Environmental Microbiology, Third Edition C. J. Hurst, R. L. Crawford, J. L. Garland, A. L. Mills, L. D. Stetzenbach, Eds. (ASM Press, Washington D.C., 2007) pp. 575-590
16. C. Tamburini, in Life as we know it. Series: Cellular Origin and Life in Extreme Habitats and Astrobiology. (Springer, Dordrecht, The Netherlands 2006) pp. 125-143