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29
38. Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV,
Naeem S. Annually reoccurring bacterial communities are pre-dictable
from ocean conditions. Proc Natl Acad Sci USA.
2006;103:13104–9.
39. Countway PD, Vigil PD, Schnetzer A, Moorthi SD, Caron DA.
Seasonal analysis of protistan community structure and diversity
at the USC Microbial Observatory (San Pedro Channel, North
Pacific Ocean). Limnol Oceanogr. 2010;55:2381–96.
40. Bruland KW, Rue EL, Smith GJ. Iron and macronutrients in
California coastal upwelling regimes: Implications for diatom
blooms. Limnol Oceanogr. 2001;46:1661–74.
41. Sunda W, Price N, Morel F, Andersen R. Trace metal metal ion
buffers. Algal Culturing Techniques: Burlington, MA; 2005, p.
35–3.
42. Bernhardt JR, Sunday JM, Thompson PL, O’Connor MI. Non-linear
averaging of thermal experience predicts population growth
rates in a thermally variable environment. Proc Biol Sci.
2018;285:20181076–10.
43. Fu F-X, Warner ME, Zhang Y, Feng Y, Hutchins DA. Effects of
increased temperature and CO2 on photosynthesis, growth, and
elemental ratios in marine Synechococcus and Prochlorococcus
(Cyanobacteria). J Phycol. 2007;43:485–96.
44. Hutchins DA, DiTullio GR, Zhang Y, Bruland KW. An iron
limitation mosaic in the California upwelling regime. Limnol
Oceanogr. 1998;43:1037–54.
45. JD Strickland, TR Parsons. A practical handbook of seawater
analysis. In: Stevenson JC, editor. Ottawa, Canada: Department of
Fisheries and the Environment Fisheries and Marine Service
Scientific Information and Publications Branch; 2012. p. 65–70.
46. Solórzano L, Sharp JH. Determination of total dissolved phos-phorus
and particulate phosphorus in natural waters. Limnol
Oceanogr. 1980;25:754–8.
47. Xu K, Fu F-X, Hutchins DA. Comparative responses of two
dominant Antarctic phytoplankton taxa to interactions between
ocean acidification, warming, irradiance, and iron availability.
Limnol Oceanogr. 2014;59:1919–31.
48. Parada AE, Needham DM, Fuhrman JA. Every base matters:
assessing small subunit rRNA primers for marine microbiomes
with mock communities, time series and global field samples.
Environ Microbiol. 2016;18:1403–14.
49. Needham DM, Fuhrman JA. Pronounced daily succession of
phytoplankton, archaea and bacteria following a spring bloom.
Nat Microbiol. 2016;1:1–7.
50. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA,
Holmes SP. DADA2: High-resolution sample inference from
Illumina amplicon data. Nat Meth. 2016;13:581–3.
51. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al.
The SILVA ribosomal RNA gene database project: improved data
processing and web-based tools. Nucleic Acids Res. 2012;41(D1):
D590–6.
52. Decelle J, Romac S, Stern RF, Bendif EM, Zingone A, Audic S,
et al. PhytoREF: a reference database of the plastidial 16S rRNA
gene of photosynthetic eukaryotes with curated taxonomy. Mol
Ecol Resour. 2015;15:1435–45.
53. Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, et al.
The Protist Ribosomal Reference database (PR2): a catalog of
unicellular eukaryote small sub-unit rRNA sequences with curated
taxonomy. Nucleic Acids Res. 2012;41(D1):D597–D604.
54. Prokopowich CD, Gregory TR, Crease TJ. The correlation
between rDNA copy number and genome size in eukaryotes.
Genome. 2003;46:48–50.
55. Green BR. Chloroplast genomes of photosynthetic eukaryotes.
Plant J. 2011;66:34–44.
56. Mizrahi-Man O, Davenport ER, Gilad Y. Taxonomic classification
of bacterial 16S rRNA genes using short sequencing reads: eva-luation
of effective study designs. PLoS One. 2013;8:e53608–14.
57. R Core Team. R: A language and environment for statistical
computing. R J 2018.
58. Racine J. RStudio: a platform-independent IDE for R and Sweave.
J Appl Econ. 2012;27:167–72.
59. McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible
interactive analysis and graphics of microbiome census data. PLoS
ONE. 2013;8:e61217–11.
60. Oksanen J, Guillaume B, Friendly M, Kindt R, Legendre P,
McGlinn D, et al. Vegan: a community ecology. R package ver-sion
2018; p. 1–297.
61. Love MI, Huber W, Anders S. Moderated estimation of fold
change and dispersion for RNA-seq data with DESeq2. Genome
Biol. 2014;15:31–21.
62. Kartal B, Van Niftrik L, Rattray J, Van De Vossenberg JL, Schmid
MC, Sinninghe Damsté J, Jetten MS, Strous M. Candidatus ‘Bro-cadia
fulgida’: an autofluorescent anaerobic ammonium oxidizing
bacterium. FEMS Microbiol Ecol. 2008;63:46–55.
63. Dąbek P. et al. Towards a multigene phylogeny of the Cymato-siraceae
(Bacillariophyta, Mediophyceae) I: novel taxa within the
subfamily Cymatosiroideae based on molecular and morphologi-cal
data. J Phycol. 2017;53:342–60.
64. Kuwata A, Yamada K, Ichinomiya M, Yoshikawa S, Tragin M,
Vaulot D. et al. Bolidophyceae, a sister picoplanktonic group of
diatoms—a review. Front Mar Sci. 2018;5:257–17.
65. Grossart H-P, Levold F, Allgaier M, Simon M, Brinkhoff T.
Marine diatom species harbour distinct bacterial communities.
Environ Microbiol. 2005;7:860–73.
66. Sohn JH, Lee J-H, Yi H, Chun J, Bae KS, Ahn T-Y, et al. Kordia
algicida gen. nov., sp. nov., an algicidal bacterium isolated from
red tide. Int J Syst Evol Microbiol. 2004;54(Pt 3):675–80.
67. Tont SA. Variability of diatom species populations: from days to
years. J Mar Res. 1987;45:985–1006.
68. Schnetzer A, Miller PE, Schaffner RA, Stauffer BA, Jones BH,
Weisberg SB, et al. Blooms of Pseudo-nitzschia and domoic
acid in the San Pedro Channel and Los Angeles harbor areas of
the Southern California Bight, 2003–2004. Harmful Algae.
2007;6:372–87.
69. Lemonnier H, Lantoine F, Courties C, Guillebault D, Nézan E,
Chomérat N. et al. Dynamics of phytoplankton communities in
eutrophying tropical shrimp ponds affected by vibriosis. Mar
Pollut Bull. 2016;110:449–59.
70. Martinez EA. Sensitivity of marine ciliates (Protozoa, Ciliophora)
to high thermal stress. Estuar Coast Mar Sci. 1980;10:369–IN1.
71. Sittenfeld A. Characterization of a photosynthetic Euglena strain
isolated from an acidic hot mud pool of a volcanic area of Costa
Rica. FEMS Microbiol Ecol. 2002;42:151–61.
72. Thomas MK, Aranguren-Gassis M, Kremer CT, Gould MR,
Anderson K, Klausmeier CA, et al. Temperature-nutrient inter-actions
exacerbate sensitivity to warming in phytoplankton. Glob.
Chang Biol. 2017;23:3269–80.
73. Jiang H-B, Fu F-X, Rivero-Calle S, Levine NM, Sañudo-Wilhelmy
SA, Qu P-P, et al. Ocean warming alleviates iron limitation of
marine nitrogen fixation. Nat Clim Change. 2018;8:1–5.
74. Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, de
Bettignies T, et al. An extreme climatic event alters marine eco-system
structure in a global biodiversity hotspot. Nat Clim Chang.
2012;5:1–5.
75. Siegle MR, Taylor EB, O’Connor MI. Prior heat accumulation
reduces survival during subsequent experimental heat waves. J
Exp Mar Bio Ecol. 2018;501:109–17.
J. D. Kling et al.
Object Description
| Title | Thermal diversity within marine phytoplankton communities |
| Author | Kling, Joshua David |
| Author email | Joshuakl@usc.edu;Joshuakl@berkeley.edu |
| Degree | Doctor of Philosophy |
| Document type | Dissertation |
| Degree program | Biology (Marine Biology and Biological Oceanography) |
| School | College of Letters, Arts and Sciences |
| Date defended/completed | 2020-08-11 |
| Date submitted | 2020-08-11 |
| Date approved | 2020-08-11 |
| Restricted until | 2020-08-11 |
| Date published | 2020-08-11 |
| Advisor (committee chair) | Hutchins, David |
| Advisor (committee member) |
Levine, Naomi Heidelberg, John Ehrenreich, Ian |
| Abstract | Marine photosynthetic carbon fixation in the sunlit upper reaches of the ocean is almost entirely carried out by chlorophyll-containing, single-celled microorganisms, and is responsible for half of the net primary production on the planet. Because of this connection to the marine carbon cycle, it is essential to assess the responses of marine phytoplankton to global change. However, this work is challenged by the dazzling diversity of both eukaryotic and prokaryotic lineages which coexist in complex phytoplankton assemblages. My dissertation contributes to this effort by investigating how the diversity of phytoplankton influences their resilience to rising temperatures. In my first study, I used natural California coastal communities collected across three seasons to show that the phytoplankton assemblage as a whole was able to maintain growth well above typical temperature ranges. However, either steady or fluctuating temperatures exceeding the maximum threshold recorded in a decade-long observational dataset caused drastic rearrangements in the phytoplankton community, including the appearance of novel dominant species. My dissertation work also highlights that there are still unrecognized but environmentally-important taxa with bizarre and unexpected life histories and thermal responses, even in the most well-studied environments. In my second study, I characterized a recently isolated nanoplanktonic diatom from the Narragansett Bay Time Series that occupies a distinct low-light, low-temperature niche. This isolate demonstrated an unusual sensitivity to light, whereby its ability to respond to what should be favorable increases in temperature is constrained by light intensity. Six years of amplicon sequencing data from the time series site suggest that this diatom is a temperate wintertime/early spring specialist, and will likely not fare well in a warmer and more stratified future ocean. In addition to expanding knowledge of functional diversity at the species level, my work also examines the potential of intra-specific diversity to house hidden adaptations to rising temperatures. Natural microbial populations are composed of distinct individual strains, whose relative abilities to contribute to the success of the whole population in a changing environment have not been well-studied. In my third study, I compared the thermal responses of 11 strains of the marine unicellular cyanobacterium Synechococcus simultaneously isolated from a single estuarine water sample to explore this cryptic intra-specific diversity. Surprisingly, these nearly genetically-identical strains showed distinct low and high temperature phenotypes. This study indicates that strain-level variation could be a key yet understudied element in the responses of phytoplankton to global change. Together, these studies highlight that the diversity of marine phytoplankton at the species and individual level includes both functional variability and redundancy relative to temperature. We can expect community composition to change over time in a warming ocean, reflecting the increasing abundance of preadapted groups or individual strains; however, wherever there are winners there are also losers. Besides providing new insights into the contribution of diversity to climate resilience, this dissertation also highlights the need to expand our knowledge of functional thermal traits, especially for typically under-studied pico- and nanoplankton which are often only known from sequence data. |
| Keyword | thermal response; phytoplankton; community ecology |
| Language | English |
| Part of collection | University of Southern California dissertations and theses |
| Publisher (of the original version) | University of Southern California |
| Place of publication (of the original version) | Los Angeles, California |
| Publisher (of the digital version) | University of Southern California. Libraries |
| Provenance | Electronically uploaded by the author |
| Type | texts |
| Legacy record ID | usctheses-m |
| Contributing entity | University of Southern California |
| Rights | Kling, Joshua David |
| Physical access | The author retains rights to his/her dissertation, thesis or other graduate work according to U.S. copyright law. Electronic access is being provided by the USC Libraries in agreement with the author, as the original true and official version of the work, but does not grant the reader permission to use the work if the desired use is covered by copyright. It is the author, as rights holder, who must provide use permission if such use is covered by copyright. The original signature page accompanying the original submission of the work to the USC Libraries is retained by the USC Libraries and a copy of it may be obtained by authorized requesters contacting the repository e-mail address given. |
| Repository name | University of Southern California Digital Library |
| Repository address | USC Digital Library, University of Southern California, University Park Campus MC 7002, 106 University Village, Los Angeles, California 90089-7002, USA |
| Repository email | cisadmin@lib.usc.edu |
| Filename | etd-KlingJoshu-8915.pdf |
| Archival file | Volume13/etd-KlingJoshu-8915.pdf |
Description
| Title | Page 34 |
| Full text | 29 38. Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV, Naeem S. Annually reoccurring bacterial communities are pre-dictable from ocean conditions. Proc Natl Acad Sci USA. 2006;103:13104–9. 39. Countway PD, Vigil PD, Schnetzer A, Moorthi SD, Caron DA. Seasonal analysis of protistan community structure and diversity at the USC Microbial Observatory (San Pedro Channel, North Pacific Ocean). Limnol Oceanogr. 2010;55:2381–96. 40. Bruland KW, Rue EL, Smith GJ. Iron and macronutrients in California coastal upwelling regimes: Implications for diatom blooms. Limnol Oceanogr. 2001;46:1661–74. 41. Sunda W, Price N, Morel F, Andersen R. Trace metal metal ion buffers. Algal Culturing Techniques: Burlington, MA; 2005, p. 35–3. 42. Bernhardt JR, Sunday JM, Thompson PL, O’Connor MI. Non-linear averaging of thermal experience predicts population growth rates in a thermally variable environment. Proc Biol Sci. 2018;285:20181076–10. 43. Fu F-X, Warner ME, Zhang Y, Feng Y, Hutchins DA. Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria). J Phycol. 2007;43:485–96. 44. Hutchins DA, DiTullio GR, Zhang Y, Bruland KW. An iron limitation mosaic in the California upwelling regime. Limnol Oceanogr. 1998;43:1037–54. 45. JD Strickland, TR Parsons. A practical handbook of seawater analysis. In: Stevenson JC, editor. Ottawa, Canada: Department of Fisheries and the Environment Fisheries and Marine Service Scientific Information and Publications Branch; 2012. p. 65–70. 46. Solórzano L, Sharp JH. Determination of total dissolved phos-phorus and particulate phosphorus in natural waters. Limnol Oceanogr. 1980;25:754–8. 47. Xu K, Fu F-X, Hutchins DA. Comparative responses of two dominant Antarctic phytoplankton taxa to interactions between ocean acidification, warming, irradiance, and iron availability. Limnol Oceanogr. 2014;59:1919–31. 48. Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14. 49. Needham DM, Fuhrman JA. Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom. Nat Microbiol. 2016;1:1–7. 50. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Meth. 2016;13:581–3. 51. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012;41(D1): D590–6. 52. Decelle J, Romac S, Stern RF, Bendif EM, Zingone A, Audic S, et al. PhytoREF: a reference database of the plastidial 16S rRNA gene of photosynthetic eukaryotes with curated taxonomy. Mol Ecol Resour. 2015;15:1435–45. 53. Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, et al. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 2012;41(D1):D597–D604. 54. Prokopowich CD, Gregory TR, Crease TJ. The correlation between rDNA copy number and genome size in eukaryotes. Genome. 2003;46:48–50. 55. Green BR. Chloroplast genomes of photosynthetic eukaryotes. Plant J. 2011;66:34–44. 56. Mizrahi-Man O, Davenport ER, Gilad Y. Taxonomic classification of bacterial 16S rRNA genes using short sequencing reads: eva-luation of effective study designs. PLoS One. 2013;8:e53608–14. 57. R Core Team. R: A language and environment for statistical computing. R J 2018. 58. Racine J. RStudio: a platform-independent IDE for R and Sweave. J Appl Econ. 2012;27:167–72. 59. McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217–11. 60. Oksanen J, Guillaume B, Friendly M, Kindt R, Legendre P, McGlinn D, et al. Vegan: a community ecology. R package ver-sion 2018; p. 1–297. 61. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:31–21. 62. Kartal B, Van Niftrik L, Rattray J, Van De Vossenberg JL, Schmid MC, Sinninghe Damsté J, Jetten MS, Strous M. Candidatus ‘Bro-cadia fulgida’: an autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol Ecol. 2008;63:46–55. 63. Dąbek P. et al. Towards a multigene phylogeny of the Cymato-siraceae (Bacillariophyta, Mediophyceae) I: novel taxa within the subfamily Cymatosiroideae based on molecular and morphologi-cal data. J Phycol. 2017;53:342–60. 64. Kuwata A, Yamada K, Ichinomiya M, Yoshikawa S, Tragin M, Vaulot D. et al. Bolidophyceae, a sister picoplanktonic group of diatoms—a review. Front Mar Sci. 2018;5:257–17. 65. Grossart H-P, Levold F, Allgaier M, Simon M, Brinkhoff T. Marine diatom species harbour distinct bacterial communities. Environ Microbiol. 2005;7:860–73. 66. Sohn JH, Lee J-H, Yi H, Chun J, Bae KS, Ahn T-Y, et al. Kordia algicida gen. nov., sp. nov., an algicidal bacterium isolated from red tide. Int J Syst Evol Microbiol. 2004;54(Pt 3):675–80. 67. Tont SA. Variability of diatom species populations: from days to years. J Mar Res. 1987;45:985–1006. 68. Schnetzer A, Miller PE, Schaffner RA, Stauffer BA, Jones BH, Weisberg SB, et al. Blooms of Pseudo-nitzschia and domoic acid in the San Pedro Channel and Los Angeles harbor areas of the Southern California Bight, 2003–2004. Harmful Algae. 2007;6:372–87. 69. Lemonnier H, Lantoine F, Courties C, Guillebault D, Nézan E, Chomérat N. et al. Dynamics of phytoplankton communities in eutrophying tropical shrimp ponds affected by vibriosis. Mar Pollut Bull. 2016;110:449–59. 70. Martinez EA. Sensitivity of marine ciliates (Protozoa, Ciliophora) to high thermal stress. Estuar Coast Mar Sci. 1980;10:369–IN1. 71. Sittenfeld A. Characterization of a photosynthetic Euglena strain isolated from an acidic hot mud pool of a volcanic area of Costa Rica. FEMS Microbiol Ecol. 2002;42:151–61. 72. Thomas MK, Aranguren-Gassis M, Kremer CT, Gould MR, Anderson K, Klausmeier CA, et al. Temperature-nutrient inter-actions exacerbate sensitivity to warming in phytoplankton. Glob. Chang Biol. 2017;23:3269–80. 73. Jiang H-B, Fu F-X, Rivero-Calle S, Levine NM, Sañudo-Wilhelmy SA, Qu P-P, et al. Ocean warming alleviates iron limitation of marine nitrogen fixation. Nat Clim Change. 2018;8:1–5. 74. Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, de Bettignies T, et al. An extreme climatic event alters marine eco-system structure in a global biodiversity hotspot. Nat Clim Chang. 2012;5:1–5. 75. Siegle MR, Taylor EB, O’Connor MI. Prior heat accumulation reduces survival during subsequent experimental heat waves. J Exp Mar Bio Ecol. 2018;501:109–17. J. D. Kling et al. |
