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28
Publisher’s note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.
References
1. Falkowski P, Barber R, Smetacek V. Biogeochemical controls and
feedbacks on ocean primary production. Science. 1998;281:200–7.
2. Hutchins DA, Fu F. Microorganisms and ocean global change.
Nat Microbiol. 2017;2:17058.
3. Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M.
Global temperature change. Proc Natl Acad Sci USA.
2006;103:14288–93.
4. Tripati AK, Roberts CD, Eagle RA. Coupling of CO2 and ice
sheet stability over major climate transitions of the last 20 million
years. Science. 2009;326:1394–7.
5. Levitus S, Antonov JI, Boyer TP, Locarnini RA, Garcia HE,
Mishonov AV. Global ocean heat content 1955–2008 in light of
recently revealed instrumentation problems. Geophys Res Lett.
2009;36:1–7.
6. IPCC. Climate change 2013: The physical science basis.
In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK,
Boschung J, et al., editors. Contribution of Working Group I to
the Fifth Assessment Report of the Intergovernmental Panel on
Climate Change. Cambridge: Cambridge University Press; 2013.
7. Eppley RW. Temperature and phytoplankton growth in the sea.
Fish Bull. 1972;70:1063–85.
8. Raven JA, Geider RJ. Temperature and algal growth. New Phytol.
1988;110:441–61.
9. Norberg J. Biodiversity and ecosystem functioning: a complex
adaptive systems approach. Limnol Oceanogr. 2004;49:1269–77.
10. Thomas MK, Kremer CT, Klausmeier CA, Litchman E. A global
pattern of thermal adaptation in marine phytoplankton. Science.
2012;338:1085–8.
11. Boyd PW, Rynearson TA, Armstrong EA, Fu F, Hayashi K, Hu Z,
et al. Marine phytoplankton temperature versus growth responses
from polar to tropical waters—outcome of a scientific community-wide
study. PLoS ONE. 2013;8:e63091–17.
12. Fu FX, Yu E, Garcia NS, Gale J, Luo Y, Webb EA, et al. Dif-fering
responses of marine N2 fixers to warming and con-sequences
for future diazotroph community structure. Aquat
Micro Ecol. 2014;72:33–46.
13. Gittings JA, Raitsos DE, Krokos G, Hoteit I. Impacts of warming
on phytoplankton abundance and phenology in a typical tropical
marine ecosystem. Sci Rep. 2018;8:1–12.
14. Poloczanska ES, Burrows MT, Brown CJ, García Molinos J,
Halpern BS, Hoegh-Guldberg O, et al. Responses of marine
organisms to climate change across oceans. Front Mar Sci.
2016;3:515–21.
15. Yvon-Durocher G, Montoya JM, Trimmer M, Woodward G.
Warming alters the size spectrum and shifts the distribution of bio-mass
in freshwater ecosystems. Glob Change Biol.
2010;17:1681–94.
16. Benner I, Diner RE, Lefebvre SC, Li D, Komada T, Carpenter EJ,
et al. Emiliania huxleyi increases calcification but not expression
of calcification-related genes in long-term exposure to elevated
temperature and pCO2. Philos Trans R Soc Lond, B, Biol Sci.
2013;368:20130049–9.
17. Hare CE, Leblanc K, DiTullio GR, Kudela RM, Zhang Y, Lee
PA, et al. Consequences of increased temperature and CO2 for
phytoplankton community structure in the Bering Sea. Mar Ecol
Prog Ser. 2007;352:9–16.
18. Feng Y, Hare CE, Leblanc K, Rose JM, Zhang Y, DiTullio GR,
et al. Effects of increased pCO2 and temperature on the North
Atlantic spring bloom. I. The phytoplankton community and
biogeochemical response. Mar Ecol Prog Ser. 2009;388:13–25.
19. Lewandowska A, Sommer U. Climate change and the spring
bloom: a mesocosm study on the influence of light and tempera-ture
on phytoplankton and mesozooplankton. Mar Ecol Prog Ser.
2010;405:101–11.
20. Hinder SL, Hays GC, Edwards M, Roberts EC, Walne AW,
Gravenor MB. Changes in marine dinoflagellate and diatom
abundance under climate change. Nat Clim Change. 2012;2:271–5.
21. Zhu Z, Xu K, Fu F, Spackeen JL, Bronk DA, Hutchins DA. A
comparative study of iron and temperature interactive effects on
diatoms and Phaeocystis antarctica from the Ross Sea, Antarctica.
Mar Ecol Prog Ser. 2016;550:39–51.
22. Kremp A, Godhe A, Egardt J, Dupont S, Suikkanen S, Casabianca
S, et al. Intraspecific variability in the response of bloom-forming
marine microalgae to changed climate conditions. Ecol Evol.
2012;2:1195–207.
23. Canesi KL, Rynearson TA. Temporal variation of Skeletonema
community composition from a long-term time series in Narra-gansett
Bay identified using high-throughput DNA sequencing.
Mar Ecol Prog Ser. 2016;556:1–16.
24. Demory D, Baudoux A-C, Monier A, Simon N, Six C, Ge P, et al.
Picoeukaryotes of the Micromonas genus: sentinels of a warming
ocean. ISME J. 2018;305:1–15.
25. Leinweber A, Gruber N, Frenzel H, Friederich GE, Chavez FP.
Diurnal carbon cycling in the surface ocean and lower atmosphere
of Santa Monica Bay, California. Geophys Res Lett. 2009;36:
L08601–5.
26. Doblin MA, van Sebille E. Drift in ocean currents impacts inter-generational
microbial exposure to temperature. Proc Natl Acad
Sci USA. 2016;13:5700–5.
27. Salinger MJ. Climate variability and change: past, present and
future—an overview. Clim Change. 2005;70:9–29.
28. Williams IN, Torn MS, Riley WJ, Wehner MF. Impacts of climate
extremes on gross primary production under global warming.
Environ Res Lett. 2014;9:1–12.
29. Vasseur DA, DeLong JP, Gilbert B, Greig HS, Harley CDG,
McCann KS, et al. Increased temperature variation poses a greater
risk to species than climate warming. Proc Biol Sci.
2014;281:20132612–2.
30. Kremer CT, Fey SB, Arellano AA, Vasseur DA. Gradual plasti-city
alters population dynamics in variable environments: thermal
acclimation in the green alga Chlamydomonas reinhartdii. Proc
Biol Sci. 2018;285:20171942–9.
31. Rasconi S, Winter K, Kainz MJ. Temperature increase and fluc-tuation
induce phytoplankton biodiversity loss—evidence from a
multi-seasonal mesocosm experiment. Ecol Evol. 2017;7:2936–46.
32. Kremer CT, Klausmeier CA. Species packing in eco-evolutionary
models of seasonally fluctuating environments. Ecol Lett.
2017;20:1158–68.
33. Schaum C-E, Rost B, Collins S. Environmental stability affects
phenotypic evolution in a globally distributed marine pico-plankton.
ISME J. 2016;10:75–84.
34. Schaum C-E, Buckling A, Smirnoff N, Studholme DJ, Yvon-
Durocher G. Environmental fluctuations accelerate molecular
evolution of thermal tolerance in a marine diatom. Nat Commun.
2018;9:1719. https://doi.org/10.1038/s41467-018-03906-5.
35. Qu P, Fu F-X, Kling J, Huh M, Wang X, Hutchins DA. Distinct
responses of Trichodesmium to a thermally-variable environment
as a function of phosphorus availability. Front Microbiol.
2019;10:1282. https://doi.org/10.3389/fmicb.2019.01282.
36. Mantyla AW, Bograd SJ, Venrick EL. Patterns and controls of
chlorophyll-a and primary productivity cycles in the Southern
California Bight. J Mar Syst. 2008;73:48–60.
37. Nezlin NP, Sutula MA, Stumpf RP, Sengupta A. Phytoplankton
blooms detected by SeaWiFS along the central and southern
California coast. J Geophys Res. 2012;117:308–17.
Transient exposure to novel high temperatures reshapes coastal phytoplankton communities
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 33 |
| Full text | 28 Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. References 1. Falkowski P, Barber R, Smetacek V. Biogeochemical controls and feedbacks on ocean primary production. Science. 1998;281:200–7. 2. Hutchins DA, Fu F. Microorganisms and ocean global change. Nat Microbiol. 2017;2:17058. 3. Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M. Global temperature change. Proc Natl Acad Sci USA. 2006;103:14288–93. 4. Tripati AK, Roberts CD, Eagle RA. Coupling of CO2 and ice sheet stability over major climate transitions of the last 20 million years. Science. 2009;326:1394–7. 5. Levitus S, Antonov JI, Boyer TP, Locarnini RA, Garcia HE, Mishonov AV. Global ocean heat content 1955–2008 in light of recently revealed instrumentation problems. Geophys Res Lett. 2009;36:1–7. 6. IPCC. Climate change 2013: The physical science basis. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, et al., editors. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press; 2013. 7. Eppley RW. Temperature and phytoplankton growth in the sea. Fish Bull. 1972;70:1063–85. 8. Raven JA, Geider RJ. Temperature and algal growth. New Phytol. 1988;110:441–61. 9. Norberg J. Biodiversity and ecosystem functioning: a complex adaptive systems approach. Limnol Oceanogr. 2004;49:1269–77. 10. Thomas MK, Kremer CT, Klausmeier CA, Litchman E. A global pattern of thermal adaptation in marine phytoplankton. Science. 2012;338:1085–8. 11. Boyd PW, Rynearson TA, Armstrong EA, Fu F, Hayashi K, Hu Z, et al. Marine phytoplankton temperature versus growth responses from polar to tropical waters—outcome of a scientific community-wide study. PLoS ONE. 2013;8:e63091–17. 12. Fu FX, Yu E, Garcia NS, Gale J, Luo Y, Webb EA, et al. Dif-fering responses of marine N2 fixers to warming and con-sequences for future diazotroph community structure. Aquat Micro Ecol. 2014;72:33–46. 13. Gittings JA, Raitsos DE, Krokos G, Hoteit I. Impacts of warming on phytoplankton abundance and phenology in a typical tropical marine ecosystem. Sci Rep. 2018;8:1–12. 14. Poloczanska ES, Burrows MT, Brown CJ, García Molinos J, Halpern BS, Hoegh-Guldberg O, et al. Responses of marine organisms to climate change across oceans. Front Mar Sci. 2016;3:515–21. 15. Yvon-Durocher G, Montoya JM, Trimmer M, Woodward G. Warming alters the size spectrum and shifts the distribution of bio-mass in freshwater ecosystems. Glob Change Biol. 2010;17:1681–94. 16. Benner I, Diner RE, Lefebvre SC, Li D, Komada T, Carpenter EJ, et al. Emiliania huxleyi increases calcification but not expression of calcification-related genes in long-term exposure to elevated temperature and pCO2. Philos Trans R Soc Lond, B, Biol Sci. 2013;368:20130049–9. 17. Hare CE, Leblanc K, DiTullio GR, Kudela RM, Zhang Y, Lee PA, et al. Consequences of increased temperature and CO2 for phytoplankton community structure in the Bering Sea. Mar Ecol Prog Ser. 2007;352:9–16. 18. Feng Y, Hare CE, Leblanc K, Rose JM, Zhang Y, DiTullio GR, et al. Effects of increased pCO2 and temperature on the North Atlantic spring bloom. I. The phytoplankton community and biogeochemical response. Mar Ecol Prog Ser. 2009;388:13–25. 19. Lewandowska A, Sommer U. Climate change and the spring bloom: a mesocosm study on the influence of light and tempera-ture on phytoplankton and mesozooplankton. Mar Ecol Prog Ser. 2010;405:101–11. 20. Hinder SL, Hays GC, Edwards M, Roberts EC, Walne AW, Gravenor MB. Changes in marine dinoflagellate and diatom abundance under climate change. Nat Clim Change. 2012;2:271–5. 21. Zhu Z, Xu K, Fu F, Spackeen JL, Bronk DA, Hutchins DA. A comparative study of iron and temperature interactive effects on diatoms and Phaeocystis antarctica from the Ross Sea, Antarctica. Mar Ecol Prog Ser. 2016;550:39–51. 22. Kremp A, Godhe A, Egardt J, Dupont S, Suikkanen S, Casabianca S, et al. Intraspecific variability in the response of bloom-forming marine microalgae to changed climate conditions. Ecol Evol. 2012;2:1195–207. 23. Canesi KL, Rynearson TA. Temporal variation of Skeletonema community composition from a long-term time series in Narra-gansett Bay identified using high-throughput DNA sequencing. Mar Ecol Prog Ser. 2016;556:1–16. 24. Demory D, Baudoux A-C, Monier A, Simon N, Six C, Ge P, et al. Picoeukaryotes of the Micromonas genus: sentinels of a warming ocean. ISME J. 2018;305:1–15. 25. Leinweber A, Gruber N, Frenzel H, Friederich GE, Chavez FP. Diurnal carbon cycling in the surface ocean and lower atmosphere of Santa Monica Bay, California. Geophys Res Lett. 2009;36: L08601–5. 26. Doblin MA, van Sebille E. Drift in ocean currents impacts inter-generational microbial exposure to temperature. Proc Natl Acad Sci USA. 2016;13:5700–5. 27. Salinger MJ. Climate variability and change: past, present and future—an overview. Clim Change. 2005;70:9–29. 28. Williams IN, Torn MS, Riley WJ, Wehner MF. Impacts of climate extremes on gross primary production under global warming. Environ Res Lett. 2014;9:1–12. 29. Vasseur DA, DeLong JP, Gilbert B, Greig HS, Harley CDG, McCann KS, et al. Increased temperature variation poses a greater risk to species than climate warming. Proc Biol Sci. 2014;281:20132612–2. 30. Kremer CT, Fey SB, Arellano AA, Vasseur DA. Gradual plasti-city alters population dynamics in variable environments: thermal acclimation in the green alga Chlamydomonas reinhartdii. Proc Biol Sci. 2018;285:20171942–9. 31. Rasconi S, Winter K, Kainz MJ. Temperature increase and fluc-tuation induce phytoplankton biodiversity loss—evidence from a multi-seasonal mesocosm experiment. Ecol Evol. 2017;7:2936–46. 32. Kremer CT, Klausmeier CA. Species packing in eco-evolutionary models of seasonally fluctuating environments. Ecol Lett. 2017;20:1158–68. 33. Schaum C-E, Rost B, Collins S. Environmental stability affects phenotypic evolution in a globally distributed marine pico-plankton. ISME J. 2016;10:75–84. 34. Schaum C-E, Buckling A, Smirnoff N, Studholme DJ, Yvon- Durocher G. Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom. Nat Commun. 2018;9:1719. https://doi.org/10.1038/s41467-018-03906-5. 35. Qu P, Fu F-X, Kling J, Huh M, Wang X, Hutchins DA. Distinct responses of Trichodesmium to a thermally-variable environment as a function of phosphorus availability. Front Microbiol. 2019;10:1282. https://doi.org/10.3389/fmicb.2019.01282. 36. Mantyla AW, Bograd SJ, Venrick EL. Patterns and controls of chlorophyll-a and primary productivity cycles in the Southern California Bight. J Mar Syst. 2008;73:48–60. 37. Nezlin NP, Sutula MA, Stumpf RP, Sengupta A. Phytoplankton blooms detected by SeaWiFS along the central and southern California coast. J Geophys Res. 2012;117:308–17. Transient exposure to novel high temperatures reshapes coastal phytoplankton communities |
