Dryland biological soil crust cyanobacteria show unexpected decreases in abundance under long-term elevated CO2.

Biological soil crusts (biocrusts) cover soil surfaces in many drylands globally. The impacts of 10 years of elevated atmospheric CO2 on the cyanobacteria in biocrusts of an arid shrubland were examined at a large manipulated experiment in Nevada, USA. Cyanobacteria-specific quantitative PCR surveys of cyanobacteria small-subunit (SSU) rRNA genes suggested a reduction in biocrust cyanobacterial biomass in the elevated CO2 treatment relative to the ambient controls. Additionally, SSU rRNA gene libraries and shotgun metagenomes showed reduced representation of cyanobacteria in the total microbial community. Taxonomic composition of the cyanobacteria was similar under ambient and elevated CO2 conditions, indicating the decline was manifest across multiple cyanobacterial lineages. Recruitment of cyanobacteria sequences from replicate shotgun metagenomes to cyanobacterial genomes representing major biocrust orders also suggested decreased abundance of cyanobacteria sequences across the majority of genomes tested. Functional assignment of cyanobacteria-related shotgun metagenome sequences indicated that four subsystem categories, three related to oxidative stress, were differentially abundant in relation to the elevated CO2 treatment. Taken together, these results suggest that elevated CO2 affected a generalized decrease in cyanobacteria in the biocrusts and may have favoured cyanobacteria with altered gene inventories for coping with oxidative stress.

[1]  N. Ward,et al.  Pyrosequencing of plastid 23S rRNA genes reveals diverse and dynamic cyanobacterial and algal populations in two eutrophic lakes. , 2012, FEMS microbiology ecology.

[2]  C. Kuske,et al.  Increased temperature and altered summer precipitation have differential effects on biological soil crusts in a dryland ecosystem , 2012 .

[3]  C. Field,et al.  Microbial communities and their responses to simulated global change fluctuate greatly over multiple years , 2012 .

[4]  R. B. Jackson,et al.  Common bacterial responses in six ecosystems exposed to 10 years of elevated atmospheric carbon dioxide. , 2012, Environmental microbiology.

[5]  C. Kuske,et al.  Targeted and shotgun metagenomic approaches provide different descriptions of dryland soil microbial communities in a manipulated field study. , 2012, Environmental microbiology reports.

[6]  C. Kuske,et al.  Response and resilience of soil biocrust bacterial communities to chronic physical disturbance in arid shrublands , 2011, The ISME Journal.

[7]  Lirong Song,et al.  Combined effects of carbon and phosphorus levels on the invasive cyanobacterium, Cylindrospermopsis raciborskii , 2012 .

[8]  S. Reed,et al.  Elevated CO2 did not mitigate the effect of a short-term drought on biological soil crusts , 2012, Biology and Fertility of Soils.

[9]  Eric P. Nawrocki,et al.  An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea , 2011, The ISME Journal.

[10]  R. Castenholz,et al.  Cyanobacterial Responses to UV Radiation , 2012 .

[11]  J. Belnap,et al.  Warming and increased precipitation frequency on the Colorado Plateau: implications for biological soil crusts and soil processes , 2012, Plant and Soil.

[12]  S. D. Smith,et al.  Effects of Elevated Atmospheric CO(2) on Rhizosphere Soil Microbial Communities in a Mojave Desert Ecosystem. , 2011, Journal of arid environments.

[13]  J. Johansen,et al.  Cyanobacteria in Soils from a Mojave Desert Ecosystem , 2011 .

[14]  Y. Hihara,et al.  Cross-talk between photomixotrophic growth and CO(2) -concentrating mechanism in Synechocystis sp. strain PCC 6803. , 2011, Environmental microbiology.

[15]  C. Kuske,et al.  Genome of the Cyanobacterium Microcoleus vaginatusFGP-2, a Photosynthetic Ecosystem Engineer of Arid Land Soil Biocrusts Worldwide , 2011, Journal of bacteriology.

[16]  A. Fairlamb,et al.  Methylglyoxal metabolism in trypanosomes and leishmania , 2011, Seminars in cell & developmental biology.

[17]  Zhengwei Zhu,et al.  FR-HIT, a very fast program to recruit metagenomic reads to homologous reference genomes , 2011, Bioinform..

[18]  B. Haas,et al.  Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. , 2011, Genome research.

[19]  F. Rodríguez-Valera,et al.  The bacterial pan-genome:a new paradigm in microbiology. , 2010, International microbiology : the official journal of the Spanish Society for Microbiology.

[20]  F. Chen,et al.  Experimental factors affecting PCR-based estimates of microbial species richness and evenness , 2010, The ISME Journal.

[21]  M. Ikeuchi,et al.  Genomic Structure of an Economically Important Cyanobacterium, Arthrospira (Spirulina) platensis NIES-39 , 2010, DNA research : an international journal for rapid publication of reports on genes and genomes.

[22]  Robert G. Beiko,et al.  Identifying biologically relevant differences between metagenomic communities , 2010, Bioinform..

[23]  I-Min A. Chen,et al.  The integrated microbial genomes system: an expanding comparative analysis resource , 2009, Nucleic Acids Res..

[24]  V. Kunin,et al.  Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. , 2009, Environmental microbiology.

[25]  H. Bolhuis,et al.  Horizontal transfer of the nitrogen fixation gene cluster in the cyanobacterium Microcoleus chthonoplastes , 2010, The ISME Journal.

[26]  D. Antonopoulos,et al.  Using the metagenomics RAST server (MG-RAST) for analyzing shotgun metagenomes. , 2010, Cold Spring Harbor protocols.

[27]  John Beardall,et al.  Living in a high CO2 world: impacts of global climate change on marine phytoplankton , 2009 .

[28]  C. Sobrino,et al.  Elevated CO2 increases sensitivity to ultraviolet radiation in lacustrine phytoplankton assemblages , 2009 .

[29]  Tracy K. Teal,et al.  Systematic artifacts in metagenomes from complex microbial communities , 2009, The ISME Journal.

[30]  Martin Hartmann,et al.  Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities , 2009, Applied and Environmental Microbiology.

[31]  U. Riebesell,et al.  Influence of elevated CO 2 concentrations on cell division and nitrogen fixation rates in the bloom-forming cyanobacterium Nodularia spumigena , 2009 .

[32]  J. Beardall,et al.  Interactions between the impacts of ultraviolet radiation, elevated CO_2, and nutrient limitation on marine primary producers , 2009, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[33]  A. Schwabe,et al.  Community Assembly of Biological Soil Crusts of Different Successional Stages in a Temperate Sand Ecosystem, as Assessed by Direct Determination and Enrichment Techniques , 2009, Microbial Ecology.

[34]  Mihai Pop,et al.  Statistical Methods for Detecting Differentially Abundant Features in Clinical Metagenomic Samples , 2009, PLoS Comput. Biol..

[35]  S. Prober,et al.  Frequent fire promotes diversity and cover of biological soil crusts in a derived temperate grassland , 2009, Oecologia.

[36]  Andreas Wilke,et al.  phylogenetic and functional analysis of metagenomes , 2022 .

[37]  S. Flint,et al.  Global change and biological soil crusts: effects of ultraviolet augmentation under altered precipitation regimes and nitrogen additions , 2008 .

[38]  C. Sobrino,et al.  Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: Effects on growth, photosynthesis, and spectral sensitivity of photoinhibition , 2008 .

[39]  Lawrence E. Page,et al.  Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina , 2008, Proceedings of the National Academy of Sciences.

[40]  Jindong Zhao,et al.  RbrA, a cyanobacterial rubrerythrin, functions as a FNR‐dependent peroxidase in heterocysts in protection of nitrogenase from damage by hydrogen peroxide in Anabaena sp. PCC 7120 , 2007, Molecular microbiology.

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

[42]  W. Ludwig,et al.  SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB , 2007, Nucleic acids research.

[43]  Fei-xue Fu,et al.  CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: Implications for past, present, and future ocean biogeochemistry , 2007 .

[44]  Fei-xue Fu,et al.  EFFECTS OF INCREASED TEMPERATURE AND CO2 ON PHOTOSYNTHESIS, GROWTH, AND ELEMENTAL RATIOS IN MARINE SYNECHOCOCCUS AND PROCHLOROCOCCUS (CYANOBACTERIA) 1 , 2007 .

[45]  C. Kuske,et al.  Three distinct clades of cultured heterocystous cyanobacteria constitute the dominant N2-fixing members of biological soil crusts of the Colorado Plateau, USA. , 2007, FEMS microbiology ecology.

[46]  F. Garcia-Pichel,et al.  Export of nitrogenous compounds due to incomplete cycling within biological soil crusts of arid lands. , 2007, Environmental microbiology.

[47]  S. Sudek,et al.  Structure of Trichamide, a Cyclic Peptide from the Bloom-Forming Cyanobacterium Trichodesmium erythraeum, Predicted from the Genome Sequence , 2006, Applied and Environmental Microbiology.

[48]  T. Huxman,et al.  Increases in Desert Shrub Productivity under Elevated Carbon Dioxide Vary with Water Availability , 2006, Ecosystems.

[49]  Naryttza N. Diaz,et al.  The Subsystems Approach to Genome Annotation and its Use in the Project to Annotate 1000 Genomes , 2005, Nucleic acids research.

[50]  James R. Cole,et al.  The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis , 2004, Nucleic Acids Res..

[51]  S. Long,et al.  What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. , 2004, The New phytologist.

[52]  Song Li,et al.  LUCY2: an interactive DNA sequence quality trimming and vector removal tool , 2004, Bioinform..

[53]  D. Ellsworth,et al.  Functional responses of plants to elevated atmospheric CO2– do photosynthetic and productivity data from FACE experiments support early predictions? , 2004 .

[54]  C. Kuske,et al.  Diazotrophic Community Structure and Function in Two Successional Stages of Biological Soil Crusts from the Colorado Plateau and Chihuahuan Desert , 2004, Applied and Environmental Microbiology.

[55]  J. Coleman,et al.  ELEVATED ATMOSPHERIC CO2 DOES NOT CONSERVE SOIL WATER IN THE MOJAVE DESERT , 2004 .

[56]  Mark E. Miller,et al.  Response of desert biological soil crusts to alterations in precipitation frequency , 2004, Oecologia.

[57]  B. Averhoff,et al.  Type IV pili-related natural transformation systems: DNA transport in mesophilic and thermophilic bacteria , 2003, Archives of Microbiology.

[58]  Jayne Belnap,et al.  The world at your feet: desert biological soil crusts , 2003 .

[59]  J. Belnap,et al.  Biological Soil Crusts: Structure, Function, and Management , 2003, Ecological Studies.

[60]  J. Johansen,et al.  PHYLOGENY AND GENETIC VARIANCE IN TERRESTRIAL MICROCOLEUS (CYANOPHYCEAE) SPECIES BASED ON SEQUENCE ANALYSIS OF THE 16S rRNA GENE AND ASSOCIATED 16S–23S ITS REGION 1 , 2002 .

[61]  J. Mattick Type IV pili and twitching motility. , 2002, Annual review of microbiology.

[62]  S. Reed,et al.  Temporal Variation in Community Composition, Pigmentation, and Fv/Fm of Desert Cyanobacterial Soil Crusts , 2002, Microbial Ecology.

[63]  F. Garcia-Pichel,et al.  Phylogenetic and Morphological Diversity of Cyanobacteria in Soil Desert Crusts from the Colorado Plateau , 2001, Applied and Environmental Microbiology.

[64]  O. Lange Photosynthesis of Soil-Crust Biota as Dependent on Environmental Factors , 2001 .

[65]  O. Lange,et al.  Biological Soil Crusts and Ecosystem Nitrogen and Carbon Dynamics , 2001 .

[66]  J. Coleman,et al.  Elevated CO2 increases productivity and invasive species success in an arid ecosystem , 2000, Nature.

[67]  J. Coleman,et al.  Biotic, abiotic and performance aspects of the Nevada Desert Free‐Air CO2 Enrichment (FACE) Facility , 1999 .

[68]  G. Muyzer,et al.  Copyright © 1997, American Society for Microbiology PCR Primers To Amplify 16S rRNA Genes from Cyanobacteria , 1997 .

[69]  J. Belnap,et al.  MICROENVIRONMENTS AND MICROSCALE PRODUCTIVITY OF CYANOBACTERIAL DESERT CRUSTS 1 , 1996 .

[70]  R. Castenholz,et al.  CHARACTERIZATION AND BIOLOGICAL IMPLICATIONS OF SCYTONEMIN, A CYANOBACTERIAL SHEATH PIGMENT 1 , 1991 .

[71]  I. Bancroft,et al.  Physical and genetic maps of the genome of the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 , 1989, Journal of bacteriology.