Biophysical model of prokaryotic diversity in geothermal hot springs.

Recent studies of photosynthetic bacteria living in geothermal hot spring environments have revealed surprisingly complex ecosystems with an unexpected level of genetic diversity. One case of particular interest involves the distribution along hot spring thermal gradients of genetically distinct bacterial strains that differ in their preferred temperatures for reproduction and photosynthesis. In such systems, a single variable, temperature, defines the relevant environmental variation. In spite of this, each region along the thermal gradient exhibits multiple strains of photosynthetic bacteria adapted to several distinct thermal optima, rather than a single thermal strain adapted to the local environmental temperature. Here we analyze microbiology data from several ecological studies to show that the thermal distribution data exhibit several universal features independent of location and specific bacterial strain. These include the distribution of optimal temperatures of different thermal strains and the functional dependence of the net population density on temperature. We present a simple population dynamics model of these systems that is highly constrained by biophysical data and by physical features of the environment. This model can explain in detail the observed thermal population distributions, as well as certain features of population dynamics observed in laboratory studies of the same organisms.

[1]  D. M. Ward A natural species concept for prokaryotes. , 1998, Current opinion in microbiology.

[2]  D. M. Ward,et al.  Genomics, environmental genomics and the issue of microbial species , 2008, Heredity.

[3]  G. Muyzer,et al.  Matching molecular diversity and ecophysiology of benthic cyanobacteria and diatoms in communities along a salinity gradient. , 2000, Environmental microbiology.

[4]  R. Rosenfeld Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[5]  Sarah Mae Sincero Heredity , 1875, Nature.

[6]  S. Hagen Exponential growth of bacteria: Constant multiplication through division , 2010 .

[7]  D. M. Ward,et al.  Cyanobacterial ecotypes in the microbial mat community of Mushroom Spring (Yellowstone National Park, Wyoming) as species-like units linking microbial community composition, structure and function , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[8]  D. M. Ward Microbial diversity in natural environments: focusing on fundamental questions , 2006, Antonie van Leeuwenhoek.

[9]  R. Ramaley,et al.  Types and distribution of obligate thermophilic bacteria in man-made and natural thermal gradients. , 1975, Applied microbiology.

[10]  R. Cavicchioli Extremophiles and the search for extraterrestrial life. , 2002, Astrobiology.

[11]  Y. Peerapornpisal,et al.  The distribution of cyanobacteria across physical and chemical gradients in hot springs in northern Thailand. , 2005, FEMS microbiology ecology.

[12]  P. Eriksson The Precambrian earth : tempos and events , 2004 .

[13]  M. Madigan,et al.  Brock Biology of Microorganisms , 1996 .

[14]  Physics Letters , 1962, Nature.

[15]  T. D. Brock Thermophilic Microorganisms and Life at High Temperatures , 1978, Springer Series in Microbiology.

[16]  N. Pace,et al.  Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[17]  H L Houtzager,et al.  Antonie van Leeuwenhoek. , 1983, European journal of obstetrics, gynecology, and reproductive biology.

[18]  J. Kuever,et al.  Relative abundance of Archaea and Bacteria along a thermal gradient of a shallow-water hydrothermal vent quantified by rRNA slot-blot hybridization. , 2000, Microbiology.

[19]  A. Watson,et al.  Biological homeostasis of the global environment: the parable of Daisyworld , 1983 .

[20]  D. M. Ward,et al.  Diverse Thermus species inhabit a single hot spring microbial mat. , 1995, Systematic and applied microbiology.

[21]  T. D. Brock,et al.  Ecological studies of Chloroflexis, a gliding photosynthetic bacterium , 1973, Archiv für Mikrobiologie.

[22]  J. Schijf,et al.  Geochimica et Cosmochimica Acta , 2008 .

[23]  D. M. Ward,et al.  Highly Ordered Vertical Structure ofSynechococcus Populations within the One-Millimeter-Thick Photic Zone of a Hot Spring Cyanobacterial Mat , 2000, Applied and Environmental Microbiology.

[24]  Jon Norberg,et al.  A general multi-trait-based framework for studying the effects of biodiversity on ecosystem functioning. , 2007, Journal of theoretical biology.

[25]  R. Castenholz,et al.  Diversity of phototrophic bacteria in microbial mats from Arctic hot springs (Greenland). , 2007, Environmental microbiology.

[26]  Eric Garnier,et al.  From Plant Traits to Plant Communities: A Statistical Mechanistic Approach to Biodiversity , 2006, Science.

[27]  D. M. Ward,et al.  Enrichment culture and microscopy conceal diverse thermophilic Synechococcus populations in a single hot spring microbial mat habitat , 1996, Applied and environmental microbiology.

[28]  D. M. Ward,et al.  Photosynthate partitioning and fermentation in hot spring microbial mat communities , 1996, Applied and environmental microbiology.

[29]  T. D. Brock Micro-organisms adapted to High Temperatures , 1967, Nature.

[30]  Yoshinari Tanaka,et al.  Predicting the phenotypic response of resource-competing communities to environmental change. , 2009, Journal of theoretical biology.

[31]  Paul Stoodley,et al.  Bacterial biofilms: from the Natural environment to infectious diseases , 2004, Nature Reviews Microbiology.

[32]  David M. Ward,et al.  A Natural View of Microbial Biodiversity within Hot Spring Cyanobacterial Mat Communities , 1998, Microbiology and Molecular Biology Reviews.

[33]  G. Muyzer,et al.  The halotolerance and phylogeny of cyanobacteria with tightly coiled trichomes (Spirulina Turpin) and the description of Halospirulina tapeticola gen. nov., sp. nov. , 2000, International journal of systematic and evolutionary microbiology.

[34]  R. Castenholz,et al.  Growth and photosynthesis in an extreme thermophile, Synechococcus lividus (Cyanophyta) , 2004, Archiv für Mikrobiologie.

[35]  R. Castenholz,et al.  Temperature Strains of a Thermophilic Blue-green Alga , 1964, Nature.

[36]  S. Goldhor Ecology , 1964, The Yale Journal of Biology and Medicine.

[37]  Elena Litchman,et al.  Trait-Based Community Ecology of Phytoplankton , 2008 .

[38]  T. D. Brock,et al.  Measurement of Steady-State Growth Rates of a Thermophilic Alga Directly in Nature , 1968, Journal of bacteriology.

[39]  U. Sommer A comparison of the Droop and the Monod models of nutrient limited growth applied to natural populations of phytoplankton , 1991 .

[40]  Everett Shock,et al.  Merging Genomes with Geochemistry in Hydrothermal Ecosystems , 2002, Science.

[41]  L. Stal,et al.  Microbial Mats: Structure, Development and Environmental Significance , 2011 .

[42]  G. Muyzer,et al.  SALINITY‐DEPENDENT LIMITATION OF PHOTOSYNTHESIS AND OXYGEN EXCHANGE IN MICROBIAL MATS , 1999 .

[43]  David M. Ward,et al.  Effect of Temperature and Light on Growth of and Photosynthesis by Synechococcus Isolates Typical of Those Predominating in the Octopus Spring Microbial Mat Community of Yellowstone National Park , 2006, Applied and Environmental Microbiology.

[44]  R. Mitchell The Evolution of Thermophily in Hot Springs , 1974, The Quarterly Review of Biology.

[45]  R. Castenholz,et al.  Dynamics of Cyanobacterial and Ostracod Interactions in an Oregon Hot Spring , 1985 .

[46]  J. Kristjánsson,et al.  Distribution of Thermus spp. in Icelandic Hot Springs and a Thermal Gradient , 1983, Applied and environmental microbiology.

[47]  Pringault,et al.  Monitoring of oxygenic and anoxygenic photosynthesis in a unicyanobacterial biofilm, grown in benthic gradient chamber. , 2000, FEMS microbiology ecology.

[48]  Natalia Khuri,et al.  Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses , 2007, The ISME Journal.

[49]  S. Eykyn Microbiology , 1950, The Lancet.

[50]  G. Muyzer,et al.  The phylogeny of unicellular, extremely halotolerant cyanobacteria , 1998, Archives of Microbiology.

[51]  A. J. Lotka Elements of mathematical biology , 1956 .

[52]  D. M. Ward,et al.  Seasonal distributions of dominant 16S rRNA-defined populations in a hot spring microbial mat examined by denaturing gradient gel electrophoresis , 1997, Applied and environmental microbiology.

[53]  T. D. Brock,et al.  Temperature Optima for Algal Development in Yellowstone and Iceland Hot Springs , 1966, Nature.

[54]  R. Castenholz,et al.  Soil Microbial Community Structure across a Thermal Gradient following a Geothermal Heating Event , 2002, Applied and Environmental Microbiology.

[55]  T. Wilcox,et al.  The Quarterly Review of Biology THE EVOLUTION OF COOPERATION , 2004 .

[56]  Larry Bull On the Evolution of Multicellularity and Eusociality , 1999, Artificial Life.

[57]  M. Madigan,et al.  Adaptation by hot spring phototrophs to reduced light intensities , 1977, Archives of Microbiology.

[58]  T. D. Brock,et al.  Population ecology of Sulfolobus acidocaldarius , 1974, Archives of Microbiology.

[59]  D. M. Ward,et al.  Denaturing Gradient Gel Electrophoresis Profiles of 16 S rRNA-Defined Populations Inhabiting a Hot Spring Microbial Mat Community , 1996 .

[60]  Scott R. Miller,et al.  Evolution of Thermotolerance in Hot Spring Cyanobacteria of the Genus Synechococcus , 2000, Applied and Environmental Microbiology.

[61]  Ulf Dieckmann,et al.  Speciation along environmental gradients , 2003, Nature.

[62]  Lisa R. Moore,et al.  Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes , 1998, Nature.

[63]  Eric G. Blackman,et al.  Temperature response of Earth to the annual solar irradiance cycle , 2004 .

[64]  S. Pointing,et al.  The effects of temperature, pH and sulphide on the community structure of hyperthermophilic streamers in hot springs of northern Thailand. , 2007, FEMS microbiology ecology.