Using a two-layered sphere model to investigate the impact of gas vacuoles on the inherent optical properties of Microcystis aeruginosa

A two-layered sphere model is used to inves- tigate the impact of gas vacuoles on the inherent optical properties (IOPs) of the cyanophyte Microcystis aeruginosa. Enclosing a vacuole-like particle within a chromatoplasm shell layer significantly altered spectral scattering and in- creased backscattering. The two-layered sphere model repro- duced features in the spectral attenuation and volume scat- tering function (VSF) that have previously been attributed to gas vacuoles. This suggests the model is good at least as a first approximation for investigating how gas vacuoles alter the IOPs. Measured Rrs was used to provide a range of values for the central value of the real refractive index, 1 + , for the shell layer using measured IOPs and a radia- tive transfer model. Sufficient optical closure was obtained for 1 + between 1.1 and 1.14, which had corresponding Chl a-specific phytoplankton backscattering, b b , between 3.9 and 7.2◊ 10 3 m 2 mg 1 at 510 nm. The b b values are in close agreement with the literature and in situ particulate backscattering measurements. Rrs simulated for a population of vacuolate cells was greatly enlarged relative to a homo- geneous population. A sensitivity analysis of empirical algo- rithms for estimating Chl a in eutrophic/hypertrophic waters suggests these are robust under variable constituent concen- trations and likely to be species-sensitive. The study confirms that gas vacuoles cause significant increase in backscattering and are responsible for the high Rrs values observed in buoy- ant cyanobacterial blooms. Gas vacuoles are therefore one of the most important bio-optical substructures influencing the IOPs in phytoplankton.

[1]  M. Matthews A current review of empirical procedures of remote sensing in inland and near-coastal transitional waters , 2011 .

[2]  M. Jost,et al.  Kinetics of the assembly of gas vacuoles in the blue-green alga Microcystis aeruginosa Kuetz. emend. Elekin. , 1971, Archiv für Mikrobiologie.

[3]  K. Carder,et al.  A simple spectral solar irradiance model for cloudless maritime atmospheres , 1990 .

[4]  Lisa R. Moore,et al.  Determination of spectral absorption coefficients of particles, dissolved material and phytoplankton for discrete water samples , 2000 .

[5]  S. Aiba,et al.  Reappraisal of the so-called light shielding of gas vacuoles in Microcystis aeruginosa , 1979, Archives of Microbiology.

[6]  Milton Kerker,et al.  Scattering of Electromagnetic Waves from Two Concentric Spheres , 1951 .

[7]  Annick Bricaud,et al.  Light backscattering efficiency and related properties of some phytoplankters , 1992 .

[8]  Richard D. Robarts,et al.  Microcystis Aeruginosa and Underwater Light Attenuation in a Hypertrophic Lake (Hartbeespoort Dam, South Africa) , 1984 .

[9]  C. Reynolds,et al.  On the Annual Cycle of the Blue-Green Alga Microcystis Aeruginosa Kutz. Emend. Elenkin , 1981 .

[10]  David Doxaran,et al.  Use of a Spectralon panel to measure the downwelling irradiance signal: case studies and recommendations. , 2004, Applied optics.

[11]  M. Milham,et al.  Optical properties of ovalbumin in 0.130–2.50 μm spectral region , 2001 .

[12]  Anatoly A. Gitelson,et al.  Remote estimation of chlorophyll concentration in hyper-eutrophic aquatic systems: Model tuning and accuracy optimization , 2006 .

[13]  Guillaume Dirberg,et al.  Bio-optical properties of the marine cyanobacteria Trichodesmium spp. , 2008 .

[14]  Hester Volten,et al.  Laboratory measurements of angular distributions of light scattered by phytoplankton and silt , 1998 .

[15]  Stewart Bernard,et al.  Characterizing the Absorption Properties for Remote Sensing of Three Small Optically-Diverse South African Reservoirs , 2013, Remote. Sens..

[16]  H. Claustre,et al.  Prochlorococcus and Synechococcus: A comparative study of their optical properties in relation to their size and pigmentation , 1993 .

[17]  Stewart Bernard,et al.  Light-scattering methods for modelling algal particles as a collection of coated and/or nonspherical scatterers , 2006 .

[18]  A. Quirantes,et al.  Simulating the optical properties of phytoplankton cells using a two-layered spherical geometry , 2009 .

[19]  D. Branton,et al.  GAS VACUOLES : Light Shielding in Blue-Green Algae , 1971 .

[20]  E. Phlips,et al.  Light absorption by cyanobacteria: Implications of the colonial growth form , 1992 .

[21]  A. Walsby,et al.  Optical properties of Gas-vacuolate cells and colonies of Microcystis in relation to light Attenuation in a Turbid, Stratified Reservoir (Mount Bold Reservoir, South Australia) , 1989 .

[22]  T. J. Petzold Volume Scattering Functions for Selected Ocean Waters , 1972 .

[23]  Deyong Sun,et al.  Mechanisms of Remote-Sensing Reflectance Variability and Its Relation to Bio-Optical Processes in a Highly Turbid Eutrophic Lake: Lake Taihu (China) , 2010, IEEE Transactions on Geoscience and Remote Sensing.

[24]  William M. Balch,et al.  Light backscattering properties of marine phytoplankton: relationships to cell size, chemical composition and taxonomy , 2004 .

[25]  Arnold G. Dekker,et al.  Detection of optical water quality parameters for eutrophic waters by high resolution remote sensing , 1993 .

[26]  G. Johnsen,et al.  In vivo absorption characteristics in 10 classes of bloom-forming phytoplankton: taxonomic characteristics and responses to photoadaptation by means of discriminant and HPLC analysis , 1994 .

[27]  Annick Bricaud,et al.  Optical properties of diverse phytoplanktonic species: experimental results and theoretical interpretation , 1988 .

[28]  J. Raven THE ROLE OF VACUOLES , 1987 .

[29]  Eyvind Aas,et al.  Refractive index of phytoplankton derived from its metabolite composition , 1996 .

[30]  Alfons Zehnder,et al.  Die Gasvakuolen der BlaualgeMicrocystis aeruginosa , 1966, Schweizerische Zeitschrift für Hydrologie.

[31]  Dariusz Stramski,et al.  On the role of colloidal particles in light scattering in the ocean , 2005 .

[32]  M. Matthews,et al.  A new algorithm for detecting trophic status ( chlorophyll-a ) , cyanobacterial-dominanance , surface scums and floating vegetation in coastal and inland waters from MERIS , 2012 .

[33]  A. Walsby,et al.  An investigation into the possible light-shielding role of gas vacuoles in a planktonic blue-green alga , 1975 .

[34]  P. Mohanty,et al.  Protective effect of supplemental low intensity white light on ultraviolet-B exposure-induced impairment in cyanobacterium Spirulina platensis: formation of air vacuoles as a possible protective measure , 2005, Photosynthesis Research.

[35]  M. Jost,et al.  Morphological parameters and macromolecular organization of gas vacuole membranes of Microcystis aeruginosa Kuetz. emend. Elenkin. , 1970, Canadian journal of microbiology.

[36]  Ae Walsby,et al.  Interactions of cyanobacteria with light , 1982 .

[37]  M. Donze,et al.  Anomalous behaviour of forward and perpendicular light scattering of a cyanobacterium owing to intracellular gas vacuoles. , 1987, Cytometry.

[38]  J. Kirk,et al.  A THEORETICAL ANALYSIS OF THE CONTRIBUTION OF ALGAL CELLS TO THE ATTENUATION OF LIGHT WITHIN NATURAL WATERS , 1976 .

[39]  G. Fuhs Interferenzmikroskopische Beobachtungen an den Polyphosphatkörpern und Gasvakuolen von Cyanophyceen , 1969, Österreichische botanische Zeitschrift.

[40]  J. U. Grobbelaar,et al.  Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis , 1984, Hydrobiologia.

[41]  Collin S. Roesler Theoretical and experimental approaches to improve the accuracy of particulate absorption coefficients derived from the quantitative filter technique , 1998 .

[42]  Jun Zhao,et al.  Variations in the optical scattering properties of phytoplankton cultures. , 2012, Optics express.

[43]  A. Gitelson,et al.  ESTIMATION OF CHLOROPHYLL a FROM TIME SERIES MEASUREMENTS OF HIGH SPECTRAL RESOLUTION REFLECTANCE IN AN EUTROPHIC LAKE , 1998 .

[44]  A. Hunt,et al.  Polarized‐light scattering studies of marine Chlorella , 1989 .

[45]  J. Overbeck,et al.  Morphology and taxonomy of Oscillatoria redekei (Cyanophyta) , 1981 .

[46]  Mark R. Miller,et al.  Ocean Optics Protocols For Satellite Ocean Color Sensor Validation, Revision 4, Volume III: Radiometric Measurements and Data Analysis Protocols , 2003 .

[47]  Junsheng Li,et al.  Modeling Remote-Sensing Reflectance and Retrieving Chlorophyll-a Concentration in Extremely Turbid Case-2 Waters (Lake Taihu, China) , 2009, IEEE Transactions on Geoscience and Remote Sensing.

[48]  T. Król,et al.  A light‐scattering matrix for unicellular marine phytoplankton , 1998 .

[49]  T. Ackerman,et al.  Algorithms for the calculation of scattering by stratified spheres. , 1981, Applied optics.

[50]  A. Bricaud,et al.  Light attenuation and scattering by phytoplanktonic cells: a theoretical modeling. , 1986, Applied optics.

[51]  G. M. Hale,et al.  Optical Constants of Water in the 200-nm to 200-microm Wavelength Region. , 1973, Applied optics.

[52]  P. Ciddor Refractive index of air: new equations for the visible and near infrared. , 1996, Applied optics.

[53]  Lee Karp-Boss,et al.  INHERENT OPTICAL PROPERTIES OF NON-SPHERICAL MARINE-LIKE PARTICLES — FROM THEORY TO OBSERVATION , 2007 .

[54]  James C. Kitchen,et al.  A three‐layered sphere model of the optical properties of phytoplankton , 1992 .

[55]  M. Jost,et al.  Physiological effects of the presence and absence of gas vacuoles in the blue-green alga,Microcystis aeruginosa Kuetz. emend. Elenkin , 1976, Archives of Microbiology.

[56]  Oscar Schofield,et al.  Influence of zeaxanthin on quantum yield of photosynthesis of Synechococcus clone WH7803 (DC2) , 1989 .

[57]  C. Reynolds The Ecology of Phytoplankton , 2006 .

[58]  J. Kirk,et al.  A THEORETICAL ANALYSIS OF THE CONTRIBUTION OF ALGAL CELLS TO THE ATTENUATION OF LIGHT WITHIN NATURAL WATERS II. SPHERICAL CELLS , 1975 .

[59]  Xiaodong Zhang,et al.  The volume scattering function of natural bubble populations , 2002 .

[60]  W Scott Pegau,et al.  Spectral backscattering properties of marine phytoplankton cultures. , 2010, Optics express.

[61]  S. Bernard,et al.  Measured and modelled optical properties of particulate matter in the southern Benguela : research article , 2001 .

[62]  Scattering properties of microalgae: the effect of cell size and cell wall. , 2007, Applied optics.

[63]  Yunlin Zhang,et al.  Effect of phytoplankton community composition and cell size on absorption properties in eutrophic shallow lakes: field and experimental evidence. , 2012, Optics express.

[64]  Lin Li,et al.  Hyperspectral remote sensing of cyanobacteria in turbid productive water using optically active pigments, chlorophyll a and phycocyanin , 2008 .

[65]  R. Brown,et al.  The ultrastructure of the marine blue green alga, Trichodesmium erythraeum, with special reference to the cell wall, gas vacuoles, and cylindrical bodies , 1969, Archiv für Mikrobiologie.

[66]  Arnold G. Dekker,et al.  Analytical algorithms for lake water TSM estimation for retrospective analyses of TM and SPOT sensor data , 2002 .

[67]  Diofantos G. Hadjimitsis,et al.  Comparison of aerosol optical thickness with in situ visibility data over Cyprus , 2010 .

[68]  P. Sánchez‐Baracaldo,et al.  Timing of morphological and ecological innovations in the cyanobacteria – a key to understanding the rise in atmospheric oxygen , 2010, Geobiology.

[69]  S. Peters,et al.  Comparison of remote sensing data, model results and in situ data for total suspended matter (TSM) in the southern Frisian lakes. , 2001, The Science of the total environment.

[70]  Annick Bricaud,et al.  Optical efficiency factors of some phytoplankters1 , 1983 .

[71]  A. Walsby,et al.  Gas vesicles in actinomycetes? , 2006, Trends in microbiology.

[72]  A. Bricaud,et al.  Modeling the inherent optical properties of the ocean based on the detailed composition of the planktonic community. , 2001, Applied optics.

[73]  R W Spinrad,et al.  Relative real refractive index of marine microorganisms: a technique for flow cytometric estimation. , 1986, Applied optics.

[74]  A. Peat,et al.  Comparative structure of the gas-vacuoles of blue-green algae , 1967, Archiv für Mikrobiologie.

[75]  Kevin Winter,et al.  Remote sensing of cyanobacteria-dominant algal blooms and water quality parameters in Zeekoevlei, a small hypertrophic lake, using MERIS , 2010 .

[76]  F. Shillington,et al.  The use of equivalent size distributions of natural phytoplankton assemblages for optical modeling. , 2007, Optics express.