Spatial patterns and links between microbial community composition and function in cyanobacterial mats

We imaged reflectance and variable fluorescence in 25 cyanobacterial mats from four distant sites around the globe to assess, at different scales of resolution, spatial variabilities in the physiological parameters characterizing their photosynthetic capacity, including the absorptivity by chlorophyll a (Achl), maximum quantum yield of photosynthesis (Ymax), and light acclimation irradiance (Ik). Generally, these parameters significantly varied within individual mats on a sub-millimeter scale, with about 2-fold higher variability in the vertical than in the horizontal direction. The average vertical profiles of Ymax and Ik decreased with depth in the mat, while Achl exhibited a sub-surface maximum. The within-mat variability was comparable to, but often larger than, the between-sites variability, whereas the within-site variabilities (i.e., between samples from the same site) were generally lowest. When compared based on averaged values of their photosynthetic parameters, mats clustered according to their site of origin. Similar clustering was found when the community composition of the mats' cyanobacterial layers were compared by automated ribosomal intergenic spacer analysis (ARISA), indicating a significant link between the microbial community composition and function. Although this link is likely the result of community adaptation to the prevailing site-specific environmental conditions, our present data is insufficient to identify the main factors determining these patterns. Nevertheless, this study demonstrates that the spatial variability in the photosynthetic capacity and light acclimation of benthic phototrophic microbial communities is at least as large on a sub-millimeter scale as it is on a global scale, and suggests that this pattern of variability scaling is similar for the microbial community composition.

[1]  C. Lovelock,et al.  Elemental composition and productivity of cyanobacterial mats in an arid zone estuary in north Western Australia , 2009, Wetlands Ecology and Management.

[2]  G. Muyzer,et al.  Structural and functional analysis of a microbial mat ecosystem from a unique permanent hypersaline inland lake: 'La Salada de Chiprana' (NE Spain). , 2003, FEMS microbiology ecology.

[3]  G. Hauska,et al.  Biological Sulfide Oxidation : Sulfide-Quinone Reductase ( SQR ) , the Primary Reaction , 2001 .

[4]  M. Kühl,et al.  Irradiance and temperature regulation of oxygenic photosynthesis and O2 consumption in a hypersaline cyanobacterial mat (Solar Lake, Egypt) , 2000 .

[5]  A. Corzo,et al.  Microbenthos in a hypersaline tidal lagoon: factors affecting microhabitat, community structure and mass exchange at the sediment-water interface , 2005 .

[6]  M. Kühl,et al.  MICROENVIRONMENTAL CONTROL OF PHOTOSYNTHESIS AND PHOTOSYNTHESIS‐COUPLED RESPIRATION IN AN EPILITHIC CYANOBACTERIAL BIOFILM 1 , 1996 .

[7]  P. Falkowski.  Light-Shade Adaptation in Marine Phytoplankton , 1980 .

[8]  J. Kromkamp,et al.  Light dependence of quantum yields for PSII charge separation and oxygen evolution in eucaryotic algae , 1998 .

[9]  C. Lovelock,et al.  Nutrient exchange of extensive cyanobacterial mats in an arid subtropical wetland , 2012 .

[10]  J. Grimalt,et al.  Microbial Mats on the Orkney Islands Revisited: Microenvironment and Microbial Community Composition , 2003, Microbial Ecology.

[11]  P. Ralph,et al.  APPARENT LIGHT REQUIREMENT FOR ACTIVATION OF PHOTOSYNTHESIS UPON REHYDRATION OF DESICCATED BEACHROCK MICROBIAL MATS 1 , 2002 .

[12]  M. Kühl,et al.  Functional and structural imaging of phototrophic microbial communities and symbioses , 2008 .

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

[14]  M. Kühl.  Optical microsensors for analysis of microbial communities. , 2005, Methods in enzymology.

[15]  H. Paerl,et al.  Structural and functional responses of microbial mats to reductions in nutrient and salinity stressors in a Bahamian hypersaline lagoon , 2011 .

[16]  C. Critchley,et al.  Rapid light curves: A new fluorescence method to assess the state of the photosynthetic apparatus , 2004, Photosynthesis Research.

[17]  B. Jørgensen,et al.  Spectral light measurements in microbenthic phototrophic communities with a fiber‐optic microprobe coupled to a sensitive diode array detector , 1992 .

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

[19]  M. Kühl,et al.  Short-term temperature effects on oxygen and sulfide cycling in a hypersaline cyanobacterial mat (Solar Lake, Egypt) , 2000 .

[20]  T. Ferdelman,et al.  Community Structure and Activity of a Highly Dynamic and Nutrient-Limited Hypersaline Microbial Mat in Um Alhool Sabkha, Qatar , 2014, PloS one.

[21]  Paul Stoodley,et al.  Modular Spectral Imaging System for Discrimination of Pigments in Cells and Microbial Communities , 2008, Applied and Environmental Microbiology.

[22]  P. Legendre,et al.  vegan : Community Ecology Package. R package version 1.8-5 , 2007 .

[23]  D. D. Marais.  Biogeochemistry of hypersaline microbial mats illustrates the dynamics of modern microbial ecosystems and the early evolution of the biosphere. , 2003 .

[24]  Scott R. Miller,et al.  Variation in Sulfide Tolerance of Photosystem II in Phylogenetically Diverse Cyanobacteria from Sulfidic Habitats , 2004, Applied and Environmental Microbiology.

[25]  A. Jassby,et al.  THE RELATIONSHIP BETWEEN PHOTOSYNTHESIS AND LIGHT FOR NATURAL ASSEMBLAGES OF COASTAL MARINE PHYTOPLANKTON 1 , 1976 .

[26]  Lucas J. Stal,et al.  Cyanobacterial Mats and Stromatolites , 2000 .

[27]  M. Kühl,et al.  Regulation of photosynthesis and oxygen consumption in a hypersaline cyanobacterial mat (Camargue, France) by irradiance, temperature and salinity. , 2006, FEMS microbiology ecology.

[28]  B. Jørgensen,et al.  Conversion and conservation of light energy in a photosynthetic microbial mat ecosystem , 2010, The ISME Journal.

[29]  R. Abed,et al.  Effect of temperature on photosynthesis, oxygen consumption and sulfide production in an extremely hypersaline cyanobacterial mat , 2006 .

[30]  J. Seckbach,et al.  Microbial mats : modern and ancient microorganisms in stratified systems , 2010 .

[31]  E. Padan,et al.  Cyanobacterial Sulfide-Quinone Reductase: Cloning and Heterologous Expression , 2000, Journal of bacteriology.

[32]  B. Jørgensen,et al.  Adaptation to Hydrogen Sulfide of Oxygenic and Anoxygenic Photosynthesis among Cyanobacteria , 1986, Applied and environmental microbiology.

[33]  B. Jørgensen,et al.  Optical properties of microbial mats: Light measurements with fiber-optic microprobes , 1994 .

[34]  H. Gemerden.  Microbial mats: A joint venture , 1993 .

[35]  G. Gerdes.  What are Microbial Mats , 2010 .

[36]  M. Kühl,et al.  Bio-optical Characteristics and the Vertical Distribution of Photosynthetic Pigments and Photosynthesis in an Artificial Cyanobacterial Mat , 2000, Microbial Ecology.

[37]  M. Bidochka,et al.  Endophytic Insect-Parasitic Fungi Translocate Nitrogen Directly from Insects to Plants , 2012, Science.

[38]  B. Osborne,et al.  Light and Photosynthesis in Aquatic Ecosystems. , 1985 .

[39]  G. Muyzer,et al.  Spatial scale and the diversity of benthic cyanobacteria and diatoms in a salina , 1999, Hydrobiologia.

[40]  B. Jørgensen,et al.  The light field of microbenthic communities: Radiance distribution and microscale optics of sandy coastal sediments , 1994 .

[41]  John F. Allen,et al.  State Transitions--a Question of Balance , 2003, Science.

[42]  J. Waterbury,et al.  Generic assignments, strain histories, and properties of pure cultures of cyanobacteria , 1979 .

[43]  P. Visscher,et al.  Lithifying microbial mats in Lagoa Vermelha, Brazil: Modern Precambrian relics? , 2006 .

[44]  J. Gower.  Generalized procrustes analysis , 1975 .

[45]  R. Reid,et al.  Resistance to burial of cyanobacteria in stromatolites , 2007 .

[46]  P. Ralph,et al.  Assessment of Photosynthetic Performance of Prochloron in Lissoclinum patella in hospite by Chlorophyll Fluorescence Measurements , 1997 .

[47]  D. D. Des Marais.  Biogeochemistry of Hypersaline Microbial Mats Illustrates the Dynamics of Modern Microbial Ecosystems and the Early Evolution of the Biosphere , 2003, The Biological Bulletin.

[48]  N. Baker.  Chlorophyll fluorescence: a probe of photosynthesis in vivo. , 2008, Annual review of plant biology.

[49]  D. Campbell,et al.  Chlorophyll Fluorescence Analysis of Cyanobacterial Photosynthesis and Acclimation , 1998, Microbiology and Molecular Biology Reviews.

[50]  P. Caumette,et al.  Microbial mats in the hypersaline ponds of Mediterranean salterns (Salins-de-Giraud, France) , 1994 .

[51]  A. Boetius,et al.  Time- and sediment depth-related variations in bacterial diversity and community structure in subtidal sands , 2009, The ISME Journal.

[52]  I. Klimant,et al.  Measurement of chlorophyll fluorescence within leaves using a modified PAM Fluorometer with a fiber-optic microprobe , 2004, Photosynthesis Research.

[53]  A. Ramette.  Quantitative Community Fingerprinting Methods for Estimating the Abundance of Operational Taxonomic Units in Natural Microbial Communities , 2009, Applied and Environmental Microbiology.

[54]  M. Kühl,et al.  Light utilization efficiency in photosynthetic microbial mats. , 2012, Environmental microbiology.

[55]  W. L. Webb,et al.  Carbon dioxide exchange of Alnus rubra , 1974, Oecologia.

[56]  A. Ramette.  Multivariate analyses in microbial ecology , 2007, FEMS microbiology ecology.

[57]  W. Vermaas.  Photosynthesis and Respiration in Cyanobacteria , 2001 .

[58]  C. Sorlini,et al.  Comparison of Different Primer Sets for Use in Automated Ribosomal Intergenic Spacer Analysis of Complex Bacterial Communities , 2004, Applied and Environmental Microbiology.

[59]  B. Jørgensen,et al.  Transition from Anoxygenic to Oxygenic Photosynthesis in a Microcoleus chthonoplastes Cyanobacterial Mat , 1986, Applied and environmental microbiology.