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Functional Genomics in an Ecological and Evolutionary Context: Maximizing the Value of Genomes in Systems Biology

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Functional Genomics and Evolution of Photosynthetic Systems

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 33))

Summary

The full power of functional genomics analyses comes from studying genomes of organisms that are known to be relevant to a system, as this permits a connection between metabolic networks within and across organisms within the systems these individuals inhabit. A genome is most effectively studied in an ecological and an evolutionary context, that is, with a view towards the relationships of the individual with other individuals within species and guilds that comprise a community and that mediate community function. We use examples from our own long-term studies of microbial mat communities found between ∼50°C and ∼72°C in alkaline siliceous hot springs of Yellowstone National Park, which are constructed by cyanobacteria (Synechococcus spp.), filamentous (Chloroflexus spp., Roseiflexus spp.) and other newly discovered anoxygenic phototrophic bacteria (Candidatus Chloracidobacterium thermophilum, Chlorobi), to illustrate that (i) isolates from systems are often numerically, genetically, and physiologically unrepresentative of the ecological diversity of predominant species, (ii) seemingly small genetic differences can be extremely important when attempting to infer system function from functions of an isolate, (iii) individuals group into ecologically distinct species populations that may or may not be typified by the characteristics of an individual and its genome, and (iv) co-evolution may be important for understanding metabolic networks among individuals of different species. Metagenomics, metatranscriptomics, metaproteomics and metabolomic/stable isotope technologies will soon enable global studies of the metabolic networking from the individual to the community level of biocomplexity. To interpret the results, we will need to understand the principles of networking at all biological levels and we will be better off if our knowledge of networking within individuals is based on the study of isolates relevant to ecological systems.

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Notes

  1. 1.

     A guild is a hypothetical construct ecologists use to combine species that do the same kind of thing, but not in exactly the same way (e.g., sun- and shade-adapted plant species both do oxygenic photosynthesis).

  2. 2.

     Also called the selective enrichment culture method.

  3. 3.

     While there is debate about what to call the major sublineages of Domains and we don’t completely agree on this, the first author prefers the use of Kingdom, which is consistent with the tradition of calling Eukaryal lineages containing animals, plants and fungi Kingdoms.

Abbreviations

SSU rRNA:

small subunit ribosomal RNA

A/B-type Synechococcus :

predominant unicellular cyanobacterial genotypes in 50–72°C alkaline siliceous hot spring microbial mats

FAP:

filamentous anoxygenic phototroph

cDNA:

complementary DNA

ITS:

internal transcribed spacer (separating 16S rRNA and 23S rRNA genes)

References

  • Adams MM, Gomez-Garcia MR, Grossman AR and Bhaya D (2008) Phosphorus deprivation responses and phosphonate utilization in a thermophilic Synechococcus sp. from microbial mats. J Bacteriol 190: 8171–8184

    Article  PubMed  CAS  Google Scholar 

  • Allewalt JP, Bateson MM, Revsbech NP, Slack K and Ward DM (2006) Effect of temperature and light on growth and photosynthesis of Synechococcus isolates typical of those predominating in the Octopus Spring microbial mat community. Appl Environ Microbiol 72: 544–550

    Article  PubMed  CAS  Google Scholar 

  • Anderson KL, Tayne TA and Ward DM (1987) Formation and fate of fermentation products in hot spring cyanobacterial mats. Appl Environ Microbiol 53: 2343–2352

    PubMed  CAS  Google Scholar 

  • Bateson MM and Ward DM (1988) Photoexcretion and consumption of glycolate in a hot spring cyanobacterial mat. Appl Environ Microbiol 54: 1738–1743

    PubMed  CAS  Google Scholar 

  • Begon M, Harper JL and Townsend CR (1990) Ecology: Individuals, Populations and Communities. 2nd Ed. Blackwell Science Publishers, Cambridge, MA

    Google Scholar 

  • Bhaya D, Grossman AR, Steunou A-S, Khuri N, Cohan FM, Hamamura N, Melendrez MC, Nelson, W, Bateson MM, Ward DM and Heidelberg JF (2007) Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses. ISME J 1: 703–713

    CAS  Google Scholar 

  • Brock TD (1987) The study of microorganisms in situ: progress and problems. Soc Gen Microbiol Symp 41: 1–17

    Google Scholar 

  • Bryant DA, Garcia Costas AM, Maresca JA, Gomez Maqueo Chew A, Klatt CG, Bateson MM, Tallon LJ, Hostetler J, Nelson WC, Heidelberg JF and Ward DM (2007) “Candidatus Chloracidobacterium thermophilum”: an aerobic phototrophic acidobacterium. Science 317: 523–526

    Google Scholar 

  • Buckley MR (2004) Systems Microbiology: Beyond Microbial Genomics. Am Acad Microbiol. Washington, DC

    Google Scholar 

  • Castenholz RW (1978) The biogeography of hot spring algae through enrichment cultures. Mitt Internat Verein Limnol 21: 296–315

    Google Scholar 

  • Castenholz RW (1981) Isolation and cultivation of thermophilic cyanobacteria. In: Balows A, Trüper HG, Dworkin M, Harder W and Schleifer K-H (eds) The Prokaryotes, a Handbook on Habitats, Isolation and Identification of Bacteria, Vol. I, pp 236–246. Springer-Verlag, Berlin/Heidelberg/New York

    Google Scholar 

  • Cohan FM and Koeppel AF (2008) The origins of ecological diversity in prokaryotes. Curr Biol 18: R1024–R1034

    Article  PubMed  CAS  Google Scholar 

  • Cohan FM and Perry EB (2007) A systematics for identifying the fundamental units of bacterial diversity. Current Biology 17: R373–R386

    Article  PubMed  CAS  Google Scholar 

  • de Queiroz K (2005) A unified concept of species and its consequences for the future of taxonomy. Proc Cal Acad Sci 56(Suppl I): 196–215

    Google Scholar 

  • Ferris MJ, and Ward DM (1997) Seasonal distributions of dominant 16S rRNA-defined populations in a hot spring microbial mat examined by denaturing gradient gel electrophoresis. Appl Environ Microbiol 63: 1375–1381

    PubMed  CAS  Google Scholar 

  • Ferris MJ, Ruff-Roberts AL, Kopczynski ED, Bateson MM and Ward DM (1996) Enrichment culture and microscopy conceal diverse thermophilic Synechococcus populations in a single hot spring microbial mat habitat. Appl Environ Microbiol 62: 1045–1050

    PubMed  CAS  Google Scholar 

  • Ferris MJ, Kühl M, Wieland A and Ward DM (2003) Different light-adapted ecotypes in a 68°C Synechococcus mat community revealed by analysis of 16S-23S intervening transcribed spacer variation. Appl Environ Microbiol 69: 2893–2898

    Article  PubMed  CAS  Google Scholar 

  • Fraser C, Alm EJ, Polz MF, Spratt BG and Hanage WP (2009) The bacterial species challenge: making sense of genetic and ecological diversity. Science 323: 741–746

    Article  PubMed  CAS  Google Scholar 

  • Garcia Costas AM, Liu Z, Tomsho LP, Schuster SC, Ward DM and Bryant DA (2011) Complete genome of Candidatus Chloracidobacterium thermophilum, a chlorophyll-based phototroph belonging to the phylum Acidobacteria. Environ Microbiol, accepted upon minor revision

    Article  PubMed  CAS  Google Scholar 

  • Gibson J, Pfennig N and Waterbury JB (1984) Chloroher­peton thalassium gen. nov. et spec. nov., a non-filamentous, flexing and gliding green sulfur bacterium. Arch Microbiol 138: 96–101

    Article  PubMed  CAS  Google Scholar 

  • Klatt CG, Bryant DA and Ward DM (2007) Comparative genomics provides evidence for the 3-hydroxypropionate autotrophic pathway in filamentous anoxygenic phototrophic bacteria and in hot spring microbial mats. Environ Microbiol 9: 2067–2078

    Article  PubMed  CAS  Google Scholar 

  • Klatt CG, Wood JM, Rusch DB, Bateson MM, Hamamura N, Heidelberg JF, Grossman AR, Bhaya D, Cohan FM, Kühl M, Bryant DA and Ward DM (2011) Community ecology of hot spring cyanobacterial mats: predominant populations and their functional potential. ISME J, in press

    Google Scholar 

  • Koeppel A, Perry EB, Sikorski J, Krizanc D, Warner A, Ward DM, Rooney AP, Brambilla E, Connor N, Ratcliff RM, Nevo E and Cohan FM (2008) Identifying the fundamental units of bacterial diversity: A paradigm shift to incorporate ecology into bacterial systematics. Proc Natl Acad Sci USA 105: 2504–2509

    Article  Google Scholar 

  • Konopka A (1992) Accumulation and utilization of polysaccharide by hot-spring phototrophs during a light-dark transition. FEMS Microb Ecol 102: 27–32

    Article  CAS  Google Scholar 

  • Liu Z, Klatt CG, Wood JM, Rusch DB, Ludwig M, Wittekindt N, Tomsho LP, Schuster SC, Ward DM and Bryant DA (2011) Metatranscriptomic analyses of chlorophototrophs of a hot-spring microbial mat. ISME J, in press

    Google Scholar 

  • Madigan MT, Jung DO, Karr EA, Sattley WM, Achenbach LA and van der Meer MTJ (2005) Diversity of anoxygenic phototrophs in contrasting extreme environments. In: Inskeep WP and McDermott TR (eds) Geothermal Biology and Geochemistry in Yellowstone National Park, pp 203–219. Montana State University Publications, Bozeman MT

    Google Scholar 

  • Mayden RL (1997) A hierarchy of species concepts: the denouement in the saga of the species problem. In: Claridge MF, Dawah HA and Wilson MR (eds) Species: the Units of Biodiversity, pp 381–424. Chapman & Hall, London, UK

    Google Scholar 

  • Melendrez MC, Lange RK, Cohan FM and Ward DM (2011) Influence of molecular resolution on sequence-based discovery of ecological diversity among Synechococcus ­population in an alkaline siliceous hot spring microbial mat. Appl Environ Microbiol 77: 1359–1367

    Google Scholar 

  • Nold SC and Ward DM (1996) Photosynthate partitioning and fermentation in hot spring microbial mat communities. Appl Environ Microbiol 62: 4598–4607

    PubMed  CAS  Google Scholar 

  • Nübel U, Bateson MM, Vandieken V, Kühl M and Ward DM (2002) Microscopic examination of distribution and phenotypic properties of phylogenetically diverse Chloroflexaceae-related bacteria in hot spring microbial mats. Appl Environ Microbiol 68: 4593–4603

    Article  PubMed  Google Scholar 

  • Papke RT, Ramsing NB, Bateson MM and Ward DM (2003) Geographical isolation in hot spring cyanobacteria. Environ Microbiol 5: 650–659

    Article  PubMed  CAS  Google Scholar 

  • Ramsing NB, Ferris MJ and Ward DM (2000) Highly ordered vertical structure of Synechococcus populations within the one-millimeter thick photic zone of a hot spring cyanobacterial mat. Appl Environ Microbiol 66: 1038–1049

    Article  PubMed  CAS  Google Scholar 

  • Revsbech NP and Ward DM (1984) Microelectrode studies of interstitial water chemistry and photosynthetic activity in a hot spring microbial mat. Appl Environ Microbiol 48: 270–275

    PubMed  CAS  Google Scholar 

  • Rosenzweig ML (1995) Species diversity in space and time. University Press, Cambridge, MA

    Book  Google Scholar 

  • Santegoeds CM, Nold SC and Ward DM (1996) Denaturing gradient gel electrophoresis used to monitor the enrichment culture of aerobic chemoorganotrophic bacteria from a hot spring cyanobacterial mat. Appl Environ Microbiol 62: 3922–3928

    PubMed  CAS  Google Scholar 

  • Schemske DW and Bradshaw HD, Jr (1999) Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc Natl Acad Sci USA 96: 11910–11915

    Article  PubMed  CAS  Google Scholar 

  • Steunou A-S, Bhaya D, Bateson MM, Melendrez MC, Ward DM, Brecht E, Peters JW, Kühl M and Grossman AR (2006) In situ analysis of nitrogen fixation and metabolic switching in unicellular thermophilic cyanobacteria inhabiting hot spring microbial mats. Proc Natl Acad Sci USA 103: 2398–2403

    Article  PubMed  CAS  Google Scholar 

  • Steunou A-S, Jensen SI, Brecht E, Becraft ED, Bateson MM, Kilian O, Bhaya D, Ward DM, Peters JM, Grossman AR and Kühl M (2008) Regulation of nif gene expression and the energetics of cyanobacterial N2 fixation over the diel cycle in a hot spring microbial mat. ISME J 2: 364–378

    Google Scholar 

  • van der Meer MTJ, Schouten S, de Leeuw JW and Ward DM (2000) Autotrophy of green non-sulphur bacteria in hot spring microbial mats: biological explanations for ­isotopically heavy organic carbon in the geological record. Environ Microbiol 2: 428–435

    Article  PubMed  Google Scholar 

  • van der Meer MTJ, Schouten S, Sinninghe-Damsté JS, de Leeuw JW and Ward DM (2003) Compound-specific isotopic fractionation patterns suggest different carbon metabolisms among Chloroflexus-like bacteria in hot spring microbial mats. Appl Environ Microbiol 69: 6000–6006

    Article  PubMed  Google Scholar 

  • van der Meer MTJ, Schouten S, Bateson MM, Nübel U, Wieland A, Kühl M, de Leeuw JW, Sinninghe-Damsté JS and Ward DM (2005) Diel variations in carbon metabolism by green nonsulfur-like bacteria in alkaline silicious hot spring microbial mats from Yellowstone National Park, USA. Appl Environ Microbiol 71: 3978–3986

    Article  PubMed  Google Scholar 

  • van der Meer MTJ, Schouten S, Sinninghe Damsté JS and Ward DM (2007) Impact of carbon metabolisms on 13C signatures of cyanobacteria and green nonsulfur-like ­bacteria inhabiting a microbial mat from an alkaline siliceous hot spring in Yellowstone National Park (USA).Environ Microbiol 9: 482–491

    Google Scholar 

  • van der Meer MTJ, Klatt CG, Wood J, Bryant DA, Bateson MM, Lammerts L, Schouten S, Sinninghe Damsté JS, Madigan MT and Ward DM (2010) Cultivation and genomic, nutritional and lipid biomarker characterization of Roseiflexus strains closely related to predominant in situ populations inhabiting Yellowstone hot spring microbial mats. J Bacteriol 192: 3033–3042

    Google Scholar 

  • VanValen L (1976) Ecological species, multispecies, and oaks. Taxon 25: 233–239

    Article  Google Scholar 

  • Ward DM (1998) A natural species concept for prokaryotes. Curr Opinion Microbiol 1: 271–277

    Article  CAS  Google Scholar 

  • Ward DM (2006) A macrobiological perspective on microbial species. Microbe 1: 269–278

    Google Scholar 

  • Ward DM and Cohan FM (2005) Microbial diversity in hot spring cyanobacterial mats: pattern and prediction. In: Inskeep B and McDermott T (eds) Geothermal Biology and Geochemistry in Yellowstone National Park, pp 185–201. Montana State University Publications, Bozeman MT

    Google Scholar 

  • Ward DM, Weller R and Bateson MM (1990) 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature 345: 63–65

    Article  PubMed  CAS  Google Scholar 

  • Ward DM, Bateson MM, Ferris MJ and Nold SC (1998) A natural view of microbial biodiversity within hot spring cyanobacterial mat communities. Microbiol Mol Biol Rev 62: 1353–1370

    PubMed  CAS  Google Scholar 

  • Ward DM, Nübel U, Papke RT and McKitrick MC (2002) Natural history of microorganisms inhabiting hot spring microbial mats: clues to the origin of microbial diversity and implications for microbiology and macrobiology. In: Staley JT and Reysenbach A-L (eds) Biodiversity of Microbial Life: Foundation of Earth’s Biosphere, pp 25–48. John Wiley and Sons, NY

    Google Scholar 

  • Ward DM, Bateson MM, Ferris MJ, Kühl M, Wieland A, Koeppel A and Cohan FM (2006) 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. Phil Trans Royal Soc London (Ser. B) 361: 1997–2008

    Google Scholar 

  • Ward DM, Cohan FM, Bhaya D, Heidelberg JF, Kühl M and Grossman AR (2008) Genomics, environmental genomics and the issue of microbial species. Heredity 100: 207–219

    Article  CAS  Google Scholar 

  • Winogradsky S (1949) Microbiologie du sol. Problemes et methodes. Barneoud Freres, France

    Google Scholar 

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Acknowledgments

This research was supported by the National Science Foundation (currently from the Frontiers in Integrative Biology Research Program, EF-0328698 and the IGERT Program in Geobiological Systems, DGE 0654336), the National Aeronautics and Space Administration (most recently from the Exobiology Program, NAG5-8824, -8807 and NX09AM87G) and the U.S. Department of Energy (BER), as part of BER’s Genomic Science Program (GSP). This contribution originates from the GSP Founda­tional Scientific Focus Area (FSFA) at the Pacific Northwest National Laboratory (PNNL), contract no. 112443. We appreciate the support of the National Park Service personnel at Yellowstone National Park. DMW thanks Peter Gogarten (University of Connecticut) for helping him to understand that the value of a genome from an isolate depends on populations genetics (i.e., the relationship of the organism whose genome is under investigation to other related individuals (and their genomes) in a system). This seems obvious today, but was not known by DMW at the time because his traditional microbiology training did not acquaint him with principles of ecology and evolution. D. A. B. additionally and gratefully acknowledges support from the National Science Foundation (MCB-0523100), Dept. of Energy (DE-FG02-94ER20137), and the Joint Genome Institute for support in obtaining genomic and metatranscriptomic sequences mentioned herein.

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Authors and Affiliations

  1. Land Resources and Environmental Sciences Department, Montana State University, Bozeman, MT, 59717, USA

    David M. Ward, Christian G. Klatt & Jason Wood

  2. Department of Biology, Wesleyan University, Middletown, CT, 06459, USA

    Frederick M. Cohan

  3. Department of Biochemistry and Molecular Biology, The Pennsylvania State University, S–235 Frear Building, University Park, PA, 16802, USA

    Donald A. Bryant

  4. Department of Chemistry and Biochemistry, Montana State University, Bozeman, MT, 59717, USA

    Donald A. Bryant

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  1. David M. Ward
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  2. Christian G. Klatt
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  3. Jason Wood
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  4. Frederick M. Cohan
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  5. Donald A. Bryant
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Correspondence to David M. Ward .

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Editors and Affiliations

  1. Dept. Microbiology & Molecular Genetics, Oklahoma State University, Stillwater, 74075, Oklahoma, USA

    Robert Burnap

  2. School of Life Sciences &, Center for Bioenergy & Photosynthesis, Arizona State University, Tempe, 85287-4501, Arizona, USA

    Wim Vermaas

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Ward, D.M., Klatt, C.G., Wood, J., Cohan, F.M., Bryant, D.A. (2012). Functional Genomics in an Ecological and Evolutionary Context: Maximizing the Value of Genomes in Systems Biology. In: Burnap, R., Vermaas, W. (eds) Functional Genomics and Evolution of Photosynthetic Systems. Advances in Photosynthesis and Respiration, vol 33. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1533-2_1

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