The global impact of bacterial processes on carbon mass

Abstract. Many recent studies have identified biological material as a major fraction of ambient aerosol loading. A small fraction of these bioaerosols consist of bacteria that have attracted a lot of attention due to their role in cloud formation and adverse health effects. Current atmospheric models consider bacteria as inert quantities and neglect cell growth and multiplication. We provide here a framework to estimate the production of secondary biological aerosol (SBA) mass in clouds by microbial cell growth and multiplication. The best estimate of SBA formation rates of 3.7 Tg yr−1 is comparable to previous model estimates of the primary emission of bacteria into the atmosphere, and thus this might represent a previously unrecognized source of biological aerosol material. We discuss in detail the large uncertainties associated with our estimates based on the rather sparse available data on bacteria abundance, growth conditions, and properties. Additionally, the loss of water-soluble organic carbon (WSOC) due to microbial processes in cloud droplets has been suggested to compete under some conditions with WSOC loss by chemical (OH) reactions. Our estimates suggest that microbial and chemical processes might lead to a global loss of WSOC of 8–11 and 8–20 Tg yr−1, respectively. While this estimate is very approximate, the analysis of the uncertainties and ranges of all parameters suggests that high concentrations of metabolically active bacteria in clouds might represent an efficient sink for organics. Our estimates also highlight the urgent need for more data concerning microbial concentrations, fluxes, and activity in the atmosphere to evaluate the role of bacterial processes as net aerosol sinks or sources on various spatial and temporal scales.

[1]  Elena S. Gusareva,et al.  Microbial communities in the tropical air ecosystem follow a precise diel cycle , 2019, Proceedings of the National Academy of Sciences.

[2]  R. A. Reis,et al.  Uncovering prokaryotic biodiversity within aerosols of the pristine Amazon forest. , 2019, The Science of the total environment.

[3]  O. Magand,et al.  Global airborne microbial communities controlled by surrounding landscapes and wind conditions , 2019, Scientific Reports.

[4]  A. Delort,et al.  Effect of endogenous microbiota on the molecular composition of cloud water: a study by Fourier-transform ion cyclotron resonance mass spectrometry (FT-ICR MS) , 2019, Scientific Reports.

[5]  P. Amato,et al.  Metatranscriptomic exploration of microbial functioning in clouds , 2019, Scientific Reports.

[6]  O. Magand,et al.  Methods to Investigate the Global Atmospheric Microbiome , 2019, Front. Microbiol..

[7]  J. Reid,et al.  Assessing the airborne survival of bacteria in populations of aerosol droplets with a novel technology , 2019, Journal of the Royal Society Interface.

[8]  S. Madronich,et al.  Solar UV radiation and microbial life in the atmosphere , 2018, Photochemical and Photobiological Sciences.

[9]  T. Šantl-Temkiv,et al.  Ice Nucleation Activity and Aeolian Dispersal Success in Airborne and Aquatic Microalgae , 2018, Front. Microbiol..

[10]  V. B. Artaev,et al.  Potential for phenol biodegradation in cloud waters , 2018, Biogeosciences.

[11]  Jason A. Lechniak,et al.  Airborne Bacteria in Earth's Lower Stratosphere Resemble Taxa Detected in the Troposphere: Results From a New NASA Aircraft Bioaerosol Collector (ABC) , 2018, Front. Microbiol..

[12]  E. Wang,et al.  Concentration and Community of Airborne Bacteria in Response to Cyclical Haze Events During the Fall and Midwinter in Beijing, China , 2018, Front. Microbiol..

[13]  Luke R. Thompson,et al.  Taxon-specific aerosolization of bacteria and viruses in an experimental ocean-atmosphere mesocosm , 2018, Nature Communications.

[14]  K. Finster,et al.  Aeolian dispersal of bacteria in southwest Greenland: their sources, abundance, diversity and physiological states , 2018, FEMS microbiology ecology.

[15]  Wenke Wang,et al.  Characteristics of total airborne microbes at various air quality levels , 2018 .

[16]  L. Deguillaume,et al.  The role of transition metal ions on HOx radicals in clouds: a numerical evaluation of its impact on multiphase chemistry , 2018 .

[17]  A. Lallement Impact des processus photochimiques et biologiques sur la composition chimique du nuage , 2017 .

[18]  Franco Miglietta,et al.  Measurements and modeling of surface–atmosphere exchange of microorganisms in Mediterranean grassland , 2017 .

[19]  M. Sancelme,et al.  H 2 O 2 modulates the energetic metabolism of the cloud microbiome , 2017 .

[20]  C. Heald,et al.  A Global Assessment of Dissolved Organic Carbon in Precipitation , 2017 .

[21]  M. Riekkola,et al.  Characterization of free amino acids, bacteria and fungi in size-segregated atmospheric aerosols in boreal forest: seasonal patterns, abundances and size distributions , 2017 .

[22]  Daizhou Zhang,et al.  Bacterial abundance and viability in rainwater associated with cyclones, stationary fronts and typhoons in southwestern Japan , 2017 .

[23]  J. Rousk,et al.  Partial drying accelerates bacterial growth recovery to rewetting , 2017 .

[24]  P. Amato,et al.  Active microorganisms thrive among extremely diverse communities in cloud water , 2017, PloS one.

[25]  A. Haddrell,et al.  Aerobiology: Experimental Considerations, Observations, and Future Tools , 2017, Applied and Environmental Microbiology.

[26]  Yonggun Jun,et al.  Invariance of Initiation Mass and Predictability of Cell Size in Escherichia coli , 2017, Current Biology.

[27]  The Contribution of Bioaerosols to the Organic Carbon Budget of the Atmosphere , 2017 .

[28]  E. Boyer,et al.  Atmospheric deposition of organic carbon via precipitation , 2016 .

[29]  G. Mailhot,et al.  Siderophores in Cloud Waters and Potential Impact on Atmospheric Chemistry: Photoreactivity of Iron Complexes under Sun-Simulated Conditions. , 2016, Environmental science & technology.

[30]  Armando D. Estillore,et al.  Atmospheric chemistry of bioaerosols: heterogeneous and multiphase reactions with atmospheric oxidants and other trace gases , 2016, Chemical science.

[31]  M. Miller,et al.  Cloudiness over the Amazon rainforest: Meteorology and thermodynamics , 2016 .

[32]  B. Bohannan,et al.  Molecular Evidence for Metabolically Active Bacteria in the Atmosphere , 2016, Front. Microbiol..

[33]  F. Marcovecchio,et al.  A new method for assessing the contribution of Primary Biological Atmospheric Particles to the mass concentration of the atmospheric aerosol. , 2016, Environment international.

[34]  S. Madronich,et al.  Rethinking the global secondary organic aerosol (SOA) budget: stronger production, faster removal, shorter lifetime , 2015 .

[35]  P. Amato,et al.  Survival of microbial isolates from clouds toward simulated atmospheric stress factors , 2015 .

[36]  G. Mailhot,et al.  A better understanding of hydroxyl radical photochemical sources in cloud waters collected at the puy de Dome station - experimental versus modelled formation rates. , 2015 .

[37]  P. Amato,et al.  Survival and ice nucleation activity of bacteria as aerosols in a cloud simulation chamber , 2015 .

[38]  T. Clauss,et al.  Characterization of airborne ice-nucleation-active bacteria and bacterial fragments , 2015 .

[39]  Vic Norris,et al.  Why do bacteria divide? , 2015, Front. Microbiol..

[40]  Mehdi Layeghifard,et al.  Seasonal community succession of the phyllosphere microbiome. , 2015, Molecular plant-microbe interactions : MPMI.

[41]  C. Morris,et al.  Features of air masses associated with the deposition of Pseudomonas syringae and Botrytis cinerea by rain and snowfall , 2014, The ISME Journal.

[42]  B. Turpin,et al.  Key parameters controlling OH‐initiated formation of secondary organic aerosol in the aqueous phase (aqSOA) , 2014 .

[43]  Joyce E. Penner,et al.  Global modeling of SOA: the use of different mechanisms for aqueous-phase formation , 2013 .

[44]  J. Collett,et al.  A review of observations of organic matter in fogs and clouds: Origin, processing and fate , 2013 .

[45]  D. Rosenfeld,et al.  On the relationship between cloud contact time and precipitation susceptibility to aerosol , 2013 .

[46]  Shian-Jiann Lin,et al.  Atmospheric Sulfur Cycle Simulated in the Global Model Gocart: Model Description and Global Properties , 2013 .

[47]  Taro Kimura,et al.  A general scavenging rate constant for reaction of hydroxyl radical with organic carbon in atmospheric waters. , 2013, Environmental science & technology.

[48]  A. Bertram,et al.  High concentrations of biological aerosol particles , 2013 .

[49]  Unravelling the bacterial diversity in the atmosphere , 2013, Applied Microbiology and Biotechnology.

[50]  W. Paul Menzel,et al.  Spatial and Temporal Distribution of Clouds Observed by MODIS Onboard the Terra and Aqua Satellites , 2013, IEEE Transactions on Geoscience and Remote Sensing.

[51]  K. Finster,et al.  Viable methanotrophic bacteria enriched from air and rain can oxidize methane at cloud-like conditions , 2013, Aerobiologia.

[52]  K. Konstantinidis,et al.  Microbiome of the upper troposphere: Species composition and prevalence, effects of tropical storms, and atmospheric implications , 2012, Proceedings of the National Academy of Sciences.

[53]  P. Amato,et al.  Potential impact of microbial activity on the oxidant capacity and organic carbon budget in clouds , 2012, Proceedings of the National Academy of Sciences.

[54]  Ulrich Pöschl,et al.  Size distributions and temporal variations of biological aerosol particles in the Amazon rainforest characterized by microscopy and real-time UV-APS fluorescence techniques during AMAZE-08 , 2012 .

[55]  L. Horowitz,et al.  Evaluation of factors controlling global secondary organic aerosol production from cloud processes , 2012 .

[56]  P. Amato,et al.  Long-term features of cloud microbiology at the puy de Dôme (France) , 2012 .

[57]  N. Mahowald,et al.  Atmospheric fluxes of organic N and P to the global ocean , 2012 .

[58]  L. Horowitz,et al.  Global in-cloud production of secondary organic aerosols: Implementation of a detailed chemical mechanism in the GFDL atmospheric model AM3 , 2012 .

[59]  N. Fierer,et al.  Seasonal variability in airborne bacterial communities at a high-elevation site , 2012 .

[60]  R. Jaenicke,et al.  Primary biological aerosol particles in the atmosphere: a review , 2012 .

[61]  P. Amato,et al.  Biotransformation of methanol and formaldehyde by bacteria isolated from clouds. Comparison with radical chemistry , 2011 .

[62]  J. Harrington,et al.  The impact of microphysical parameters, ice nucleation mode, and habit growth on the ice/liquid partitioning in mixed-phase Arctic clouds , 2011 .

[63]  P. Amato,et al.  Atmospheric chemistry of carboxylic acids: microbial implication versus photochemistry , 2011 .

[64]  P. Amato,et al.  Hydrogen peroxide in natural cloud water: Sources and photoreactivity , 2011 .

[65]  R. Mcpeters,et al.  Microbial survival in the stratosphere and implications for global dispersal , 2011 .

[66]  P. Amato,et al.  Implications of subzero metabolic activity on long-term microbial survival in terrestrial and extraterrestrial permafrost. , 2010, Astrobiology.

[67]  P. Amato,et al.  A short overview of the microbial population in clouds: Potential roles in atmospheric chemistry and nucleation processes , 2010 .

[68]  S. Burrows,et al.  How important is biological ice nucleation in clouds on a global scale? , 2010 .

[69]  D. Nilsson,et al.  Annual Variations in the Diversity, Viability, and Origin of Airborne Bacteria , 2010, Applied and Environmental Microbiology.

[70]  M. Lawrence,et al.  Bacteria in the global atmosphere – Part 2: Modeling of emissions and transport between different ecosystems , 2009 .

[71]  M. Lawrence,et al.  Bacteria in the global atmosphere – Part 1: Review and synthesis of literature data for different ecosystems , 2009 .

[72]  P. Amato,et al.  Contribution of Microbial Activity to Carbon Chemistry in Clouds , 2009, Applied and Environmental Microbiology.

[73]  J. Hall,et al.  Low Salinity and High-Level UV-B Radiation Reduce Single-Cell Activity in Antarctic Sea Ice Bacteria , 2009, Applied and Environmental Microbiology.

[74]  M. Hannigan,et al.  The contribution of biological particles to observed particulate organic carbon at a remote high altitude site , 2009 .

[75]  C. Heald,et al.  Atmospheric budget of primary biological aerosol particles from fungal spores , 2009 .

[76]  U. Pöschl,et al.  High diversity of fungi in air particulate matter , 2009, Proceedings of the National Academy of Sciences.

[77]  W. Winiwarter,et al.  Quantifying emissions of primary biological aerosol particle mass in Europe , 2009 .

[78]  P. Amato,et al.  Macromolecular synthesis by yeasts under frozen conditions. , 2009, Environmental microbiology.

[79]  P. Ariya,et al.  Physical and chemical characterization of bioaerosols – Implications for nucleation processes , 2009 .

[80]  K. Carslaw,et al.  Boreal forests, aerosols and the impacts on clouds and climate , 2008, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[81]  P. Amato,et al.  Energy Metabolism Response to Low-Temperature and Frozen Conditions in Psychrobacter cryohalolentis , 2008, Applied and Environmental Microbiology.

[82]  M. Schnaiter,et al.  Heterogeneous ice nucleation activity of bacteria: new laboratory experiments at simulated cloud conditions , 2008 .

[83]  Anne Monod,et al.  Structure-activity relationship for the estimation of OH-oxidation rate constants of aliphatic organic compounds in the aqueous phase: alkanes, alcohols, organic acids and bases , 2008 .

[84]  J. Schimel,et al.  Drying and rewetting effects on C and N mineralization and microbial activity in surface and subsurface California grassland soils , 2008 .

[85]  K. Sand‐Jensen,et al.  Bacterial metabolism in small temperate streams under contemporary and future climates , 2007 .

[86]  M. Andreae,et al.  Contribution of fungi to primary biogenic aerosols in the atmosphere: wet and dry discharged spores, carbohydrates, and inorganic ions , 2007 .

[87]  P. Amato,et al.  A fate for organic acids, formaldehyde and methanol in cloud water: their biotransformation by micro-organisms , 2007 .

[88]  P. Amato,et al.  Microorganisms isolated from the water phase of tropospheric clouds at the Puy de Dôme: major groups and growth abilities at low temperatures. , 2007, FEMS microbiology ecology.

[89]  H. Engelberg-Kulka,et al.  Bacterial Programmed Cell Death and Multicellular Behavior in Bacteria , 2006, PLoS genetics.

[90]  M. Häggblom,et al.  Characterization of psychrotolerant heterotrophic bacteria from Finnish Lapland. , 2006, Systematic and applied microbiology.

[91]  R. Jaenicke Abundance of Cellular Material and Proteins in the Atmosphere , 2005, Science.

[92]  J. Peccia,et al.  Source Bioaerosol Concentration and rRNA Gene-Based Identification of Microorganisms Aerosolized at a Flood Irrigation Wastewater Reuse Site , 2005, Applied and Environmental Microbiology.

[93]  J. Elster,et al.  Growth and morphology variation as a response to changing environmental factors in two Arctic species of Raphidonema (Trebouxiophyceae) from snow and soil , 2005, Polar Biology.

[94]  C. Morris,et al.  Ice nucleation active bacteria and their potential role in precipitation , 2004 .

[95]  P. Price,et al.  Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[96]  H. Herrmann,et al.  Kinetics of aqueous phase reactions relevant for atmospheric chemistry. , 2003, Chemical reviews.

[97]  H. Bauer,et al.  Airborne bacteria as cloud condensation nuclei , 2003 .

[98]  Anne Monod,et al.  The role of transition metal ions on HO x radicals in clouds: a numerical evaluation of its impact on multiphase chemistry , 2003 .

[99]  Mark Bydder,et al.  CAPRAM 2.4 (MODAC mechanism): An extended and condensed tropospheric aqueous phase mechanism and its application , 2003 .

[100]  Stefan Bertilsson,et al.  Heterotrophic Bacterial Growth Efficiency and Community Structure at Different Natural Organic Carbon Concentrations , 2003, Applied and Environmental Microbiology.

[101]  K. Nealson,et al.  Reproduction and metabolism at − 10°C of bacteria isolated from Siberian permafrost , 2003 .

[102]  P. Ariya,et al.  Microbiological degradation of atmospheric organic compounds , 2002 .

[103]  Katarina Vrede,et al.  Elemental Composition (C, N, P) and Cell Volume of Exponentially Growing and Nutrient-Limited Bacterioplankton , 2002, Applied and Environmental Microbiology.

[104]  C. Schadt,et al.  Changes in Soil Microbial Community Structure and Function in an Alpine Dry Meadow Following Spring Snow Melt , 2002, Microbial Ecology.

[105]  Birgit Sattler,et al.  Bacterial growth in supercooled cloud droplets , 2001 .

[106]  William B. Rossow,et al.  Cloud Vertical Structure and Its Variations from a 20-Yr Global Rawinsonde Dataset , 2000 .

[107]  M. Middelboe,et al.  Bacterial Growth Rate and Marine Virus–Host Dynamics , 2000, Microbial Ecology.

[108]  Ruprecht Jaenicke,et al.  The size distribution of primary biological aerosol particles in the multiphase atmosphere , 2000 .

[109]  C. Morris,et al.  The Relationship of Host Range, Physiology, and Genotype to Virulence on Cantaloupe in Pseudomonas syringae from Cantaloupe Blight Epidemics in France. , 2000, Phytopathology.

[110]  R. Amann,et al.  Changes in community composition during dilution cultures of marine bacterioplankton as assessed by flow cytometric and molecular biological techniques. , 2000, Environmental microbiology.

[111]  P. Grady An investment for the future. , 1997, The Journal of small animal practice.

[112]  W. Whitman,et al.  Prokaryotes: the unseen majority. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[113]  P. Buseck,et al.  Wet and dry sizes of atmospheric aerosol particles: An AFM‐TEM Study , 1998 .

[114]  B. Lighthart The ecology of bacteria in the alfresco atmosphere , 1997 .

[115]  Sandro Fuzzi,et al.  Fog droplets—an atmospheric source of secondary biological aerosol particles , 1997 .

[116]  M. Kyle,et al.  Ratios of carbon, nitrogen and phosphorus in Pseudomonas fluorescens as a model for bacterial element ratios and nutrient regeneration , 1996 .

[117]  R. Jaenicke,et al.  The processing of water vapor and aerosols by atmospheric clouds, a global estimate , 1995 .

[118]  B. Lighthart,et al.  Viable bacterial aerosol particle size distributions in the midsummer atmosphere at an isolated location in the high desert chaparral , 1995 .

[119]  B. Lighthart,et al.  Bacterial flux from chaparral into the atmosphere in mid-summer at a high desert location , 1994 .

[120]  D. Kell,et al.  Dormancy in Stationary-Phase Cultures of Micrococcus luteus: Flow Cytometric Analysis of Starvation and Resuscitation , 1993, Applied and environmental microbiology.

[121]  D B Kell,et al.  Dormancy in non-sporulating bacteria. , 1993, FEMS microbiology reviews.

[122]  A. G. Marr,et al.  Growth rate of Escherichia coli. , 1991, Microbiological reviews.

[123]  P. Artaxo,et al.  Aerosol characteristics and sources for the Amazon Basin during the wet season , 1990 .

[124]  J. Lelieveld,et al.  Influences of cloud photochemical processes on tropospheric ozone , 1990, Nature.

[125]  K. Davey,et al.  A predictive model for combined temperature and water activity on microbial growth during the growth phase. , 1989, The Journal of applied bacteriology.

[126]  C. Upper,et al.  Plants as Sources of Airborne Bacteria, Including Ice Nucleation-Active Bacteria , 1982, Applied and environmental microbiology.

[127]  R. Dimmick,et al.  Evidence that bacteria can form new cells in airborne particles , 1979, Applied and environmental microbiology.

[128]  R. Roffey,et al.  Three-year investigation of the natural airborne bacterial flora at four localities in sweden , 1978, Applied and environmental microbiology.

[129]  I. Newman Aerobiology on Commercial Air Routes , 1948, Nature.