1932

Abstract

Geochemical cycles of all nonconservative elements are mediated by microorganisms over nanometer spatial scales. The pelagic seascape is known to possess microstructure imposed by heterogeneous distributions of particles, polymeric gels, biologically important chemicals, and microbes. While indispensable, most traditional oceanographic observational approaches overlook this heterogeneity and ignore subtleties, such as activity hot spots, symbioses, niche partitioning, and intrapopulation phenotypic variations, that can provide a deeper mechanistic understanding of planktonic ecosystem function. As part of the movement toward cultivation-independent tools in microbial oceanography, techniques to examine the ecophysiology of individual populations and their role in chemical transformations at spatial scales relevant to microorganisms have been developed. This review presents technologies that enable geochemical and microbiological interrogations at spatial scales ranging from 0.02 to a few hundred micrometers, particularly focusing on atomic force microscopy, nanoscale secondary ion mass spectrometry, and confocal Raman microspectroscopy and introducing promising approaches for future applications in marine sciences.

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2019-01-03
2024-06-18
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Literature Cited

  1. Abbe E 1873. Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung. Arch. Mikrosk. Anat. 9:413–18
    [Google Scholar]
  2. Ault AP, Axson JL 2017. Atmospheric aerosol chemistry: spectroscopic and microscopic advances. Anal. Chem. 89:430–52
    [Google Scholar]
  3. Azam F 1998. Microbial control of oceanic carbon flux: the plot thickens. Science 280:694–96
    [Google Scholar]
  4. Baines SB, Chen X, Vogt S, Fisher NS, Twining BS, Landry MR 2015. Microplankton trace element contents: implications for mineral limitation of mesozooplankton in an HNLC area. J. Plankton Res. 38:256–70
    [Google Scholar]
  5. Baines SB, Twining BS, Brzezinski MA, Krause JW, Vogt S et al. 2012. Significant silicon accumulation by marine picocyanobacteria. Nat. Geosci. 5:886–91
    [Google Scholar]
  6. Bar-Zeev E, Berman-Frank I, Girshevitz O, Berman T 2012. Revised paradigm of aquatic biofilm formation facilitated by microgel transparent exopolymer particles. PNAS 109:9119–24
    [Google Scholar]
  7. Barletta RE, Dikes HM 2015. Chemical analysis of sea ice vein μ-environments using Raman spectroscopy. Polar Rec 51:165–76
    [Google Scholar]
  8. Barletta RE, Krause JW, Goodie T, El Sabae H 2015. The direct measurement of intracellular pigments in phytoplankton using resonance Raman spectroscopy. Mar. Chem. 176:164–73
    [Google Scholar]
  9. Behrens S, Lösekann T, Pett-Ridge J, Weber PK, Ng WO et al. 2008. Linking microbial phylogeny to metabolic activity at the single-cell level by using enhanced element labeling-catalyzed reporter deposition fluorescence in situ hybridization (EL-FISH) and NanoSIMS. Appl. Environ. Microbiol. 74:3143–50
    [Google Scholar]
  10. Benavides M, Berthelot H, Duhamel S, Raimbault P, Bonnet S 2017. Dissolved organic matter uptake by Trichodesmium in the southwest Pacific. Sci. Rep. 7:41315
    [Google Scholar]
  11. Berg JS, Schwedt A, Kreutzmann AC, Kuypers MMM, Milucka J 2014. Polysulfides as intermediates in the oxidation of sulfide to sulfate by Beggiatoa spp. Appl. Environ. Microbiol. 80:629–36
    [Google Scholar]
  12. Berry D, Mader E, Lee TK, Woebken D, Wang Y et al. 2015. Tracking heavy water (D2O) incorporation for identifying and sorting active microbial cells. PNAS 112:E194–203
    [Google Scholar]
  13. Bertram MA, Cowen JP 1997. Morphological and compositional evidence for biotic precipitation of marine barite. J. Mar. Res. 55:577–93
    [Google Scholar]
  14. Betzig E 2015. Nobel Lecture: single molecules, cells, and super-resolution optics. Rev. Mod. Phys. 87:1153–68
    [Google Scholar]
  15. Bhatt K, Tan S, Karumuri S, Kalkan AK 2010. Charge-selective Raman scattering and fluorescence quenching by “nanometal on semiconductor” substrates. Nano Lett 10:3880–87
    [Google Scholar]
  16. Biagini GA, Hayes AJ, Suller MTE, Winters C, Finlay BJ, Lloyd D 1997. Hydrogenosomes of Metopus contortus physiologically resemble mitochondria. Microbiology 143:1623–29
    [Google Scholar]
  17. Bird DF, Kalff J 1986. Bacterial grazing by planktonic lake algae. Science 231:493–95
    [Google Scholar]
  18. Bolnick DI, Amarasekare P, Araújo MS, Bürger R, Levine JM et al. 2011. Why intraspecific trait variation matters in community ecology. Trends Ecol. Evol. 26:183–92
    [Google Scholar]
  19. Bonnet S, Berthelot H, Turk-Kubo K, Dekaezemacker J, Fawcett S et al. 2016. Diazotroph derived nitrogen supports diatom growth in the South West Pacific: a quantitative study using nanoSIMS. Limnol. Oceanogr. 61:1549–62
    [Google Scholar]
  20. Brehm-Stecher BF, Johnson EA 2004. Single-cell microbiology: tools, technologies, and applications. Microbiol. Mol. Biol. Rev. 68:538–59
    [Google Scholar]
  21. Bucci V, Nunez-Milland D, Twining BS, Hellweger FL 2012. Microscale patchiness leads to large and important intraspecific internal nutrient heterogeneity in phytoplankton. Aquat. Ecol. 46:101–18
    [Google Scholar]
  22. Burgess S, Li X, Houand J 2013. High spatial resolution energy dispersive X-ray spectrometry in the SEM and the detection of light elements including lithium. Microsc. Anal. 27:S8–13
    [Google Scholar]
  23. Canfield DE, Stewart FJ, Thamdrup B, De Brabandere L, Dalsgaard T et al. 2010. A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast. Science 330:1375–78
    [Google Scholar]
  24. Chazallon B, Focsa C, Charlou J-L, Bourry C, Donval J-P 2007. A comparative Raman spectroscopic study of natural gas hydrates collected at different geological sites. Chem. Geol 244:175–85
    [Google Scholar]
  25. Cicerone M 2016. Molecular imaging with CARS micro-spectroscopy. Curr. Opin. Chem. Biol. 33:179–85
    [Google Scholar]
  26. Craig RL, Bondy AL, Ault AP 2015. Surface-enhanced Raman spectroscopy enables observations of previously undetectable secondary organic aerosol components at the individual particle level. Anal. Chem. 87:7510–14
    [Google Scholar]
  27. Cui L, Yang K, Zhou G, Huang WE, Zhu Y-G 2017. Surface-enhanced Raman spectroscopy combined with stable isotope probing to monitor nitrogen assimilation at both bulk and single-cell level. Anal. Chem 89:5793–800
    [Google Scholar]
  28. Czarnocki-Cieciura M, Nowotny M 2016. Introduction to high-resolution cryo-electron microscopy. Postępy Biochem 62:383–94
    [Google Scholar]
  29. Danilatos GD 1994. Environmental scanning electron microscopy and microanalysis. Microchim. Acta 114:143–55
    [Google Scholar]
  30. Dekas AE, Chadwick GL, Bowles MW, Joye SB, Orphan VJ 2014. Spatial distribution of nitrogen fixation in methane seep sediment and the role of the ANME archaea. Environ. Microbiol. 16:3012–29
    [Google Scholar]
  31. Dekas AE, Connon SA, Chadwick GL, Trembath-Reichert E, Orphan VJ 2016. Activity and interactions of methane seep microorganisms assessed by parallel transcription and FISH-NanoSIMS analyses. ISME J 10:678–92
    [Google Scholar]
  32. Dekas AE, Orphan VJ 2011. Identification of diazotrophic microorganisms in marine sediment via fluorescence in situ hybridization coupled to nanoscale secondary ion mass spectrometry (FISH-NanoSIMS). Methods Enzymol 486:281–305
    [Google Scholar]
  33. DeLong EF, Wickham GS, Pace NR 1989. Phylogenetic stains: ribosomal RNA-based probes for the identification of single cells. Science 243:1360–63
    [Google Scholar]
  34. Enders K, Lenz R, Stedmon CA, Nielsen TG 2015. Abundance, size and polymer composition of marine microplastics ≥ 10 μm in the Atlantic Ocean and their modelled vertical distribution. Mar. Pollut. Bull. 100:70–81
    [Google Scholar]
  35. Estillore AD, Morris HS, Or VW, Lee HD, Alves MR et al. 2017. Linking hygroscopicity and the surface microstructure of model inorganic salts, simple and complex carbohydrates, and authentic sea spray aerosol particles. Phys. Chem. Chem. Phys. 19:21101–11
    [Google Scholar]
  36. Fike DA, Gammon CL, Ziebis W, Orphan VJ 2008. Micron-scale mapping of sulfur cycling across the oxycline of a cyanobacterial mat: a paired nanoSIMS and CARD-FISH approach. ISME J 2:749–59
    [Google Scholar]
  37. Finzi-Hart JA, Pett-Ridge J, Weber PK, Popa R, Fallon SJ et al. 2009. Fixation and fate of C and N in the cyanobacterium Trichodesmium using nanometer-scale secondary ion mass spectrometry. PNAS 106:6345–50
    [Google Scholar]
  38. Fleischmann M, Hendra PJ, McQuillan AJ 1974. Raman spectra of pyridine adsorbed at a silver electrode. Chem. Phys. Lett. 26:163–66
    [Google Scholar]
  39. Fleming Y, Wirtz T 2015. High sensitivity and high resolution element 3D analysis by a combined SIMS-SPM instrument. Beilstein J. Nanotechnol. 6:1091–99
    [Google Scholar]
  40. Foster RA, Kuypers MMM, Vagner T, Paerl RW, Musat N, Zehr JP 2011. Nitrogen fixation and transfer in open ocean diatom-cyanobacterial symbioses. ISME J 5:1484–93
    [Google Scholar]
  41. Foster RA, Sztejrenszus S, Kuypers MMM 2013. Measuring carbon and N2 fixation in field populations of colonial and free-living unicellular cyanobacteria using nanometer-scale secondary ion mass spectrometry. J. Phycol. 49:502–16
    [Google Scholar]
  42. Foster T, Clode PL 2016. Skeletal mineralogy of coral recruits under high temperature and pCO2. Biogeosciences 13:1717–22
    [Google Scholar]
  43. Gan Y 2009. Atomic and subnanometer resolution in ambient conditions by atomic force microscopy. Surf. Sci. Rep. 64:99–121
    [Google Scholar]
  44. Gebeshuber IC, Kindt JH, Thompson JB, Del Amo Y, Stachelberger H et al. 2003. Atomic force microscopy study of living diatoms in ambient conditions. J. Microsc. 212:292–99
    [Google Scholar]
  45. Hall EK, Singer GA, Pölzl M, Hämmerle I, Schwarz C et al. 2011. Looking inside the box: using Raman microspectroscopy to deconstruct microbial biomass stoichiometry one cell at a time. ISME J 5:196–208
    [Google Scholar]
  46. He S, Xie W, Zhang P, Fang S, Li Z et al. 2018. Preliminary identification of unicellular algal genus by using combined confocal resonance Raman spectroscopy with PCA and DPLS analysis. Spectrochim. Acta A 190:417–22
    [Google Scholar]
  47. Hell SW 2015. Nobel Lecture: nanoscopy with freely propagating light. Rev. Mod. Phys. 87:1169–81
    [Google Scholar]
  48. Hell SW, Dyba M, Jakobs S 2004. Concepts for nanoscale resolution in fluorescence microscopy. Curr. Opin. Neurobiol. 14:599–609
    [Google Scholar]
  49. Hellweger FL, Kianirad E 2007.a Accounting for intrapopulation variability in biogeochemical models using agent-based methods. Environ. Sci. Technol. 41:2855–60
    [Google Scholar]
  50. Hellweger FL, Kianirad E 2007.b Individual-based modeling of phytoplankton: evaluating approaches for applying the cell quota model. J. Theor. Biol. 249:554–65
    [Google Scholar]
  51. Hermelink A, Brauer A, Lasch P, Naumann D 2009. Phenotypic heterogeneity within microbial populations at the single-cell level investigated by confocal Raman microspectroscopy. Analyst 134:1149–53
    [Google Scholar]
  52. Hippius C, Nied S, Schu G, Feßenbecker A, Schürmann G et al. 2013. Surface analysis for the identification of effective strategies to fight marine biofouling. Desalin. Water Treat. 51:19443994
    [Google Scholar]
  53. Hobbie JE, Daley JR, Jasper JE 1977. Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl. Environ. Microbiol. 33:1225–28
    [Google Scholar]
  54. House CH, Orphan VJ, Turk KA, Thomas B, Pernthaler A et al. 2009. Extensive carbon isotopic heterogeneity among methane seep microbiota. Environ. Microbiol. 11:2207–15
    [Google Scholar]
  55. Huang WE, Bailey MJ, Thompson IP, Whiteley AS, Spiers AJ 2007.a Single-cell Raman spectral profiles of Pseudomonas fluorescens SBW25 reflects in vitro and in planta metabolic history. Microb. Ecol. 53:414–25
    [Google Scholar]
  56. Huang WE, Ferguson A, Singer AC, Lawson K, Thompson IP et al. 2009. Resolving genetic functions within microbial populations: in situ analyses using rRNA and mRNA stable isotope probing coupled with single-cell Raman-fluorescence in situ hybridization. Appl. Environ. Microbiol. 75:234–41
    [Google Scholar]
  57. Huang WE, Griffiths RI, Thompson IP, Bailey MJ, Whiteley AS et al. 2004. Raman microscopic analysis of single microbial cells. Anal. Chem. 76:4452–58
    [Google Scholar]
  58. Huang WE, Stoecker K, Griffiths R, Newbold L, Daims H et al. 2007.b Raman-FISH: combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function. Environ. Microbiol. 9:1878–89
    [Google Scholar]
  59. Ji Y, He Y, Cui Y, Wang T, Wang Y et al. 2014. Raman spectroscopy provides a rapid, non-invasive method for quantitation of starch in live, unicellular microalgae. Biotechnol. J. 9:1512–18
    [Google Scholar]
  60. Kang Y, Taylor GT, Gobler CJ, Tang YZ, Taylor GT, Gobler CJ 2017. Discovery of a resting stage in the harmful, brown-tide-causing pelagophyte, Aureoumbra lagunensis: a mechanism potentially facilitating recurrent blooms and geographic expansion. J. Phycol. 130:118–30
    [Google Scholar]
  61. Kawata S, Ichimura T, Taguchi A, Kumamoto Y 2017. Nano-Raman scattering microscopy: resolution and enhancement. Chem. Rev. 117:4983–5001
    [Google Scholar]
  62. King AL, Sañudo-Wilhelmy SA, Boyd PW, Twining BS, Wilhelm SW et al. 2012. A comparison of biogenic iron quotas during a diatom spring bloom using multiple approaches. Biogeosciences 9:667–87
    [Google Scholar]
  63. Knittel K, Boetius A 2009. Anaerobic oxidation of methane: progress with an unknown process. Annu. Rev. Microbiol. 63:311–34
    [Google Scholar]
  64. Kopf SH, McGlynn SE, Green-Saxena A, Guan YB, Newman DK, Orphan VJ 2015. Heavy water and 15N labelling with NanoSIMS analysis reveals growth rate-dependent metabolic heterogeneity in chemostats. Environ. Microbiol. 17:2542–56
    [Google Scholar]
  65. Krupke A, Musat N, LaRoche J, Mohr W, Fuchs BM et al. 2013. In situ identification and N2 and C fixation rates of uncultivated cyanobacteria populations. Syst. Appl. Microbiol. 36:259–71
    [Google Scholar]
  66. Kuznetsov YG, Chang S-CC, Credaroli A, Martiny J, McPherson A 2012. An atomic force microscopy investigation of cyanophage structure. Micron 43:1336–42
    [Google Scholar]
  67. Kuznetsov YG, Martiny JB, McPherson A 2010. Structural analysis of a Synechococcus myovirus S-CAM4 and infected cells by atomic force microscopy. J. Gen. Virol. 91:3095–104
    [Google Scholar]
  68. Le Ru EC, Blackie E, Meyer M, Etchegoint PG 2007. Surface enhanced Raman scattering enhancement factors: a comprehensive study. J. Phys. Chem. C 111:13794–803
    [Google Scholar]
  69. Lee HD, Estillore AD, Morris HS, Ray KK, Alejandro A et al. 2017. Direct surface tension measurements of individual sub-micrometer particles using atomic force microscopy. J. Phys. Chem. A 121:8296–305
    [Google Scholar]
  70. Lee N, Nielsen PH, Andreasen KH, Juretschko S, Nielsen JL et al. 1999. Combination of fluorescent in situ hybridization and microautoradiography—a new tool for structure-function analyses in microbial ecology. Appl. Environ. Microbiol. 65:1289–97
    [Google Scholar]
  71. Li M, Canniffe DP, Jackson PJ, Davison PA, FitzGerald S et al. 2012.a Rapid resonance Raman microspectroscopy to probe carbon dioxide fixation by single cells in microbial communities. ISME J 6:875–85
    [Google Scholar]
  72. Li M, Dang D, Xi N, Wang Y, Liu L 2017. Nanoscale imaging and force probing of biomolecular systems using atomic force microscopy: from single molecules to living cells. Nanoscale 9:17643–66
    [Google Scholar]
  73. Li M, Huang WE, Gibson CM, Fowler PW, Jousset A et al. 2012.b Stable isotope probing and Raman spectroscopy for monitoring carbon flow in a food chain and revealing metabolic pathway. Anal. Chem. 85:1642–49
    [Google Scholar]
  74. Lidstrom ME, Konopka MC 2010. The role of physiological heterogeneity in microbial population behavior. Nat. Chem. Biol. 6:705–12
    [Google Scholar]
  75. Lin X, Scranton M, Varela R, Chistoserdov A, Taylor G 2007. Compositional responses of bacterial communities to redox gradients and grazing in the anoxic Cariaco Basin. Aquat. Microb. Ecol. 47:57–72
    [Google Scholar]
  76. Lombardi JR, Birke RL 2008. A unified approach to surface-enhanced Raman spectroscopy. J. Phys. Chem. C 112:5605–17
    [Google Scholar]
  77. Losic D, Short K, Mitchell JG, Lal R, Voelcker NH 2007. AFM nanoindentations of diatom biosilica surfaces. Langmuir 23:5014–21
    [Google Scholar]
  78. Malfatti F, Azam F 2010. Atomic force microscopy reveals microscale networks and possible symbioses among pelagic marine bacteria. Aquat. Microb. Ecol. 58:1–14
    [Google Scholar]
  79. Malfatti F, Samo TJ, Azam F 2010. High-resolution imaging of pelagic bacteria by atomic force microscopy and implications for carbon cycling. ISME J 4:427–39
    [Google Scholar]
  80. Mari X, Kiørboe T 1996. Abundance, size distribution and bacterial colonization of transparent exopolymeric particles (TEP) during spring in the Kattegat. J. Plankton Res. 18:969–86
    [Google Scholar]
  81. Mattila M, Carpen L, Hakkarainen T, Salkinoja-Salonen MS 1997. Biofilm development during ennoblement of stainless steel in Baltic Sea water: a microscopic study. Int. Biodeterior. Biodegrad. 40:1–10
    [Google Scholar]
  82. Mayhew LE, Ellison ET, Miller HM, Kelemen PB, Templeton AS 2018. Iron transformations during low temperature alteration of variably serpentinized rocks from the Samail ophiolite, Oman. Geochim. Cosmochim. Acta. 222:704–28
    [Google Scholar]
  83. McEvoy AL, Greenfield D, Bates M, Liphardt J 2010. Q&A: single-molecule localization microscopy for biological imaging. BMC Biol 8:106
    [Google Scholar]
  84. Meksiarun P, Spegazzini N, Matsui H, Nakajima K, Matsuda Y, Sato H 2015. In vivo study of lipid accumulation in the microalgae marine diatom Thalassiosira pseudonana using Raman spectroscopy. Appl. Spectrosc. 69:45–51
    [Google Scholar]
  85. Moerner WE 2015. Nobel Lecture: single-molecule spectroscopy, imaging, and photocontrol: foundations for super-resolution microscopy. Rev. Mod. Phys. 87:1183–212
    [Google Scholar]
  86. Moudříková Š, Mojzeš P, Zachleder V, Pfaff C, Behrendt D, Nedbal L 2016. Raman and fluorescence microscopy sensing energy-transducing and energy-storing structures in microalgae. Algal Res 16:224–32
    [Google Scholar]
  87. Muhamadali H, Chisanga M, Subaihi A, Goodacre R 2015. Combining Raman and FT-IR spectroscopy with quantitative isotopic labeling for differentiation of E. coli cells at community and single cell levels. Anal. Chem. 87:4578–86
    [Google Scholar]
  88. Musat N, Adam B, Kuypers MMM 2011. Nano-secondary ions mass spectrometry (nanoSIMS) coupled with in situ hybridization for ecological research. Stable Isotope Probing and Related Technologies JC Murrell, AS Whiteley 295–303 Washington, DC: ASM Press
    [Google Scholar]
  89. Musat N, Foster R, Vagner T, Adam B, Kuypers MMM 2012. Detecting metabolic activities in single cells, with emphasis on nanoSIMS. FEMS Microbiol. Rev. 36:486–511
    [Google Scholar]
  90. Musat N, Halm H, Winterholler B, Hoppe P, Peduzzi S et al. 2008. A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. PNAS 105:17861–66
    [Google Scholar]
  91. Musat N, Musat F, Weber PK, Pett-Ridge J 2016. Tracking microbial interactions with NanoSIMS. Curr. Opin. Biotechnol. 41:114–21
    [Google Scholar]
  92. Musat N, Stryhanyuk H, Bombach P, Adrian L, Audinot JN, Richnow HH 2014. The effect of FISH and CARD-FISH on the isotopic composition of 13C- and 15N-labeled Pseudomonas putida cells measured by nanoSIMS. Syst. Appl. Microbiol. 37:267–76
    [Google Scholar]
  93. NARMIL (Nano-RAMAN Mol. Imaging Lab.). 2018. Instruments. Nano-RAMAN Molecular Imaging Laboratory, Stony Brook University https://you.stonybrook.edu/nanoraman/specification-2
    [Google Scholar]
  94. Noble RRT, Fuhrman JJA 1998. Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat. Microb. Ecol. 14:113–18
    [Google Scholar]
  95. Nuester J, Vogt S, Twining BS 2012. Localization of iron within centric diatoms of the genus Thalassiosira. J. Phycol 48:626–34
    [Google Scholar]
  96. Nuñez J, Renslow R, Cliff JB III, Anderton CR 2018. NanoSIMS for biological applications: current practices and analyses. Biointerphases 13:03B301
    [Google Scholar]
  97. Oren A, Mana L, Jehlička J 2015. Probing single cells of purple sulfur bacteria with Raman spectroscopy: carotenoids and elemental sulfur. FEMS Microbiol. Lett. 362:fnv021
    [Google Scholar]
  98. Orphan VJ 2009. Methods for unveiling cryptic microbial partnerships in nature. Curr. Opin. Microbiol. 12:231–37
    [Google Scholar]
  99. Orphan VJ, House CH 2009. Geobiological investigations using secondary ion mass spectrometry: microanalysis of extant and paleo-microbial processes. Geobiology 7:360–72
    [Google Scholar]
  100. Orphan VJ, House CH, Hinrichs K-U, McKeegan KD, DeLong EF 2001. Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293:484–87
    [Google Scholar]
  101. Pasulka AL, Thamatrakoln K, Kopf SH, Guan Y, Poulos B et al. 2018. Interrogating marine virus-host interactions and elemental transfer with BONCAT and nanoSIMS-based methods. Environ. Microbiol. 20:671–92
    [Google Scholar]
  102. Pätzold R, Keuntje M, Theophile K, Müller J, Mielcarek E et al. 2008. In situ mapping of nitrifiers and anammox bacteria in microbial aggregates by means of confocal resonance Raman microscopy. J. Microbiol. Methods 72:241–48
    [Google Scholar]
  103. Peng X, Guo Z, House CH, Chen S, Ta K 2016. SIMS and NanoSIMS analyses of well-preserved microfossils imply oxygen-producing photosynthesis in the Mesoproterozoic anoxic ocean. Chem. Geol. 441:24–34
    [Google Scholar]
  104. Pernthaler A, Pernthaler J, Amann R 2002. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68:3094–101
    [Google Scholar]
  105. Pletikapic G, Radic TM, Zimmermann AH, Svetlicic V, Pfannkuchen M et al. 2011. AFM imaging of extracellular polymer release by marine diatom Cylindrotheca closterium (Ehrenberg) Reiman & J.C. Lewin. J. Mol. Recognit. 24:436–45
    [Google Scholar]
  106. Polerecky L, Adam B, Milucka J, Musat N, Vagner T, Kuypers MMM 2012. Look@NanoSIMS – a tool for the analysis of nanoSIMS data in environmental microbiology. Environ. Microbiol. 14:1009–23
    [Google Scholar]
  107. Powell LC, Hilal N, Wright CJ 2017. Atomic force microscopy study of the biofouling and mechanical properties of virgin and industrially fouled reverse osmosis membranes. Desalination 404:313–21
    [Google Scholar]
  108. Prince RC, Frontiera RR, Potma EO 2017. Stimulated Raman scattering: from bulk to nano. Chem. Rev. 117:5070–94
    [Google Scholar]
  109. Rabier C, Anguy Y, Cabioch G, Genthon P 2008. Characterization of various stages of calcitization in Porites sp corals from uplifted reefs—case studies from New Caledonia, Vanuatu, and Futuna (South-West Pacific). Sediment. Geol. 211:73–86
    [Google Scholar]
  110. Raman CV, Krishnan KS 1928. A new type of secondary radiation. Nature 121:501–2
    [Google Scholar]
  111. Richard C, Mitbavkar S, Landoulsi J 2017. Diagnosis of the diatom community upon biofilm development on stainless steels in natural freshwater. Scanning 2017:5052646
    [Google Scholar]
  112. Rincón-Tomás B, Khonsari B, Mühlen D, Wickbold C, Schäfer N et al. 2016. Manganese carbonates as possible biogenic relics in Archean settings. Int. J. Astrobiol. 15:219–29
    [Google Scholar]
  113. Rüger J, Unger N, Schie IW, Brunner E, Popp J, Krafft C 2016. Assessment of growth phases of the diatom Ditylum brightwellii by FT-IR and Raman spectroscopy. Algal Res 19:246–52
    [Google Scholar]
  114. Sahoo SK, Umapathy S, Parker AW 2011. Time-resolved resonance Raman spectroscopy: exploring reactive intermediates. Appl. Spectrosc. 65:1087–115
    [Google Scholar]
  115. Santschi PH, Balnois E, Wilkinson KJ, Zhang J, Buffle J et al. 2012. Fibrillar polysaccharides in marine as imaged by atomic macromolecular organic matter force microscopy and transmission electron microscopy. Limnol. Oceanogr. 43:896–908
    [Google Scholar]
  116. Schopf JW, Kudryavtsev AB, Agresti DG, Czaja AD, Wdowiak TJ 2005. Raman imagery: a new approach to assess the geochemical maturity and biogenicity of permineralized precambrian fossils. Astrobiology 5:333–71
    [Google Scholar]
  117. Sheik AR, Brussaard CPDD, Lavik G, Foster RA, Musat N et al. 2013. Viral infection of Phaeocystis globosa impedes release of chitinous star-like structures: quantification using single cell approaches. Environ. Microbiol. 15:1441–51
    [Google Scholar]
  118. Simon M, Grossart H, Schweitzer B, Ploug H 2002. Microbial ecology of organic aggregates in aquatic ecosystems. Aquat. Microb. Ecol. 28:175–211
    [Google Scholar]
  119. Sintes E, Herndl GJ 2006. Quantifying substrate uptake by individual cells of marine bacterioplankton by catalyzed reporter deposition fluorescence in situ hybridization combined with micro autoradiography. Appl Env. Microbiol. 72:7022–28
    [Google Scholar]
  120. Smith DJ 2008. Ultimate resolution in the electron microscope?. Mater. Today 11:Suppl.30–38
    [Google Scholar]
  121. Song Y, Kaster A-K, Vollmers J, Song Y, Davison PA et al. 2017. Single-cell genomics based on Raman sorting reveals novel carotenoid-containing bacteria in the Red Sea. Microb. Biotechnol. 10:125–37
    [Google Scholar]
  122. Stocker R 2015. The 100 μm length scale in the microbial ocean. Aquat. Microb. Ecol. 76:189–94
    [Google Scholar]
  123. Stolpe B, Hassellöv M 2010. Nanofibrils and other colloidal biopolymers binding trace elements in coastal seawater: significance for variations in element size distributions. Limnol. Oceanogr. 55:187–202
    [Google Scholar]
  124. Stranahan SM, Willets KA 2010. Super-resolution optical imaging of single-molecule SERS hot spots. Nano Lett 10:3777–84
    [Google Scholar]
  125. Strommen DP, Nakamoto K 1977. Resonance Raman spectroscopy. J. Chem. Educ. 54:474–78
    [Google Scholar]
  126. Svetličić V, Žutić V, Pletikapić G, Radić TM, Svetli V et al. 2013. Marine polysaccharide networks and diatoms at the nanometric scale. Int. J. Mol. Sci. 14:20064–78
    [Google Scholar]
  127. Taylor GT, Li ZQ, Suter E, Chow S 2017.a Modified filter-transfer-freeze (“FTF”) technique for Raman microspectroscopic analysis of single cells. Protocols.io. https://doi.org/10.17504/protocols.io.ikqccvw
    [Crossref] [Google Scholar]
  128. Taylor GT, Sharma SK, Mohanan K 1990. Optimization of a flow injection sampling system for quantitative analysis of dilute aqueous solutions using combined Resonance and Surface-Enhanced Raman Spectroscopy (SERRS). Appl. Spectrosc. 44:635–40
    [Google Scholar]
  129. Taylor GT, Sullivan CW 1984. The use of 14C-labeled bacteria as a tracer of ingestion and metabolism of bacterial biomass by microbial grazers. J. Microbiol. Methods 3:101–24
    [Google Scholar]
  130. Taylor GT, Suter EA, Li ZQ, Chow S, Stinton D et al. 2017.b Single-cell growth rates in photoautotrophic populations measured by stable isotope probing and resonance Raman microspectrometry. Front. Microbiol. 8:1449
    [Google Scholar]
  131. Taylor GT, Zheng D, Lee M, Troy PJ, Gyananath G, Sharma SK 1997. Influence of surface properties on accumulation of conditioning films and marine bacteria on substrata exposed to oligotrophic waters. Biofouling 11:31–57
    [Google Scholar]
  132. Terrado R, Pasulka AL, Lie AA-Y, Orphan VJ, Heidelberg KB, Caron DA 2017. Autotrophic and heterotrophic acquisition of carbon and nitrogen by a mixotrophic chrysophyte established through stable isotope analysis. ISME J 11:2022–34
    [Google Scholar]
  133. Thompson AW, Foster RA, Krupke A, Carter BJ, Musat N et al. 2012. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337:1546–50
    [Google Scholar]
  134. Twining BS, Baines SB, Fisher NS, Maser J, Vogt S et al. 2003. Quantifying trace elements in individual aquatic protist cells with a synchrotron X-ray fluorescence microprobe. Anal. Chem. 75:3806–16
    [Google Scholar]
  135. Twining BS, Rauschenberg S, Morton PL, Vogt S 2015. Metal contents of phytoplankton and labile particulate material in the North Atlantic Ocean. Prog. Oceanogr. 137:261–83
    [Google Scholar]
  136. Ueno Y, Isozaki Y, Yurimoto H, Maruyama S 2001. Carbon isotopic signatures of individual archean microfossils(?) from western Australia. Int. Geol. Rev. 43:196–212
    [Google Scholar]
  137. Verdugo P, Alldredge AL, Azam F, Kirchman DL, Passow U, Santschi PH 2004. The oceanic gel phase: a bridge in the DOM–POM continuum. Mar. Chem. 92:67–85
    [Google Scholar]
  138. Verma P 2017. Tip-enhanced Raman spectroscopy: technique and recent advances. Chem. Rev. 117:6447–66
    [Google Scholar]
  139. Wagner M 2009. Single-cell ecophysiology of microbes as revealed by Raman microspectroscopy or secondary ion mass spectrometry imaging. Annu. Rev. Microbiol. 63:411–29
    [Google Scholar]
  140. Wagner M, Nielsen PH, Loy A, Nielsen JL, Daims H 2006. Linking microbial community structure with function: fluorescence in situ hybridization-microautoradiography and isotope arrays. Curr. Opin. Biotechnol. 17:83–91
    [Google Scholar]
  141. Walters CM, Pao C, Gagnon BP, Zamecnik CR, Walker GC 2018. Bright surface-enhanced Raman scattering with fluorescence quenching from silica encapsulated J-aggregate coated gold nanoparticles. Adv. Mater. 30:1705381
    [Google Scholar]
  142. Ward BB, Perry MJ 1980. Immunofluorescent assay for the marine ammonium-oxidizing bacterium Nitrosococcus oceanus. Appl. Environ. Microbiol 39:913–18
    [Google Scholar]
  143. Woebken D, Burow LC, Behnam F, Mayali X, Schintlmeister A et al. 2015. Revisiting N2 fixation in Guerrero Negro intertidal microbial mats with a functional single-cell approach. ISME J 9:485–96
    [Google Scholar]
  144. Worden AZ, Follows MJ, Giovannoni SJ, Wilken S, Zimmerman AE, Keeling PJ 2015. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science 347:1257594
    [Google Scholar]
  145. Xi K, Sharma SK, Taylor GT, Muenow DW 1992. Determination of low concentrations of the azo-dye complex of nitrite in fresh water and seawater using surface-enhanced resonance Raman spectroscopy (SERRS). Appl. Spectrosc. 46:819–26
    [Google Scholar]
  146. Young AM, Elliott JA 2016. Characterization of microplastic and mesoplastic debris in sediments from Kamilo Beach and Kahuku Beach, Hawai'i. Mar. Pollut. Bull. 113:477–82
    [Google Scholar]
  147. Zhang Y, Zhang F, Yang J, Jiao N 2012. Host responses of a marine bacterium, Roseobacter denitrificans OCh114, to phage infection. Arch. Microbiol. 194:323–30
    [Google Scholar]
  148. Zhao X, Schwartz CL, Pierson J, Giovannoni SJ, McIntosh JR, Nicastro D 2017. Three-dimensional structure of the ultraoligotrophic marine bacterium “Candidatus Pelagibacter ubique.”. Appl. Environ. Microbiol. 83:e02807–16
    [Google Scholar]
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