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18
The ISME Journal
https://doi.org/10.1038/s41396-019-0525-6
ARTICLE
Transient exposure to novel high temperatures reshapes coastal
phytoplankton communities
Joshua D. Kling1 ● Michael D. Lee2 ● Feixue Fu1 ● Megan D. Phan1 ● Xinwei Wang1,3 ● Pingping Qu1 ●
David A. Hutchins 1
Received: 29 March 2019 / Revised: 4 September 2019 / Accepted: 13 September 2019
© The Author(s), under exclusive licence to International Society for Microbial Ecology 2019
Abstract
Average sea surface temperatures are expected to rise 4° this century, and marine phytoplankton and bacterial community
composition, biogeochemical rates, and trophic interactions are all expected to change in a future warmer ocean. Thermal
experiments typically use constant temperatures; however, weather and hydrography cause marine temperatures to fluctuate
on diel cycles and over multiple days. We incubated natural communities of phytoplankton collected from California coastal
waters during spring, summer, and fall under present-day and future mean temperatures, using thermal treatments that were
either constant or fluctuated on a 48 h cycle. As assayed by marker-gene sequencing, the emergent microbial communities
were consistent within each season, except when culture temperatures exceeded the highest temperature recorded in a 10-
year local thermal dataset. When temperature treatments exceeded the 10-year maximum the phytoplankton community
shifted, becoming dominated by diatom amplicon sequence variants (ASVs) not seen at lower temperatures. When mean
temperatures were above the 10-year maximum, constant and fluctuating regimes each selected for different ASVs. These
findings suggest coastal microbial communities are largely adapted to the current range of temperatures they experience.
They also suggest a general hypothesis whereby multiyear upper temperature limits may represent thresholds, beyond which
large community restructurings may occur. Now inevitable future temperature increases that exceed these environmental
thresholds, even temporarily, may fundamentally reshape marine microbial communities and therefore the biogeochemical
cycles that they mediate.
Introduction
Marine phytoplankton draw down atmospheric CO2,
support marine food webs, and provide long-term
carbon storage in underlying deep waters [1]. Currently,
anthropogenic CO2 inputs are inducing changes in
phytoplankton communities by changing temperature and
climate regimes [2]. Present-day atmospheric CO2 con-centrations
of >400 ppm have not been seen for almost 12
million years, and these past elevated CO2 events were
accompanied by substantial warming [3, 4]. The high
specific heat of seawater has meant that warming of the
ocean’s surface has happened more slowly than warming
of land. Even so, global mean sea surface temperature
(SST) has gone up 0.7 °C in the last three decades, and is
expected to rise an additional 4 °C this century [3, 5, 6].
Warming influences phytoplankton growth and physiol-ogy
[7, 8]. Growth rates across temperatures for phyto-plankton
typically have thermal performance curves (TPC)
that increase gradually with rising temperatures to an opti-mal
maximum, then decrease rapidly at higher temperatures
[9]. Thermal optima and limits for species are typically
connected to in situ thermal regimes. For instance, phyto-plankton
at lower latitudes often live near their optimal
temperatures, whereas temperate species are temperature-limited
[10–12]. Because of the rapid decrease in growth
* David A. Hutchins
dahutch@usc.edu
1 Department of Biological Sciences, University of Southern
California, Los Angeles, CA 90007, USA
2 Exobiology Branch, NASA Ames Research Center, Moffett Blvd.,
Mountain View, CA 94035, USA
3 School of Life Sciences, Xiamen University, 361005
Xiamen, China
Supplementary information The online version of this article (https://
doi.org/10.1038/s41396-019-0525-6) contains supplementary
material, which is available to authorized users.
1234567890();,:
1234567890();,:
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 23 |
| Full text | 18 The ISME Journal https://doi.org/10.1038/s41396-019-0525-6 ARTICLE Transient exposure to novel high temperatures reshapes coastal phytoplankton communities Joshua D. Kling1 ● Michael D. Lee2 ● Feixue Fu1 ● Megan D. Phan1 ● Xinwei Wang1,3 ● Pingping Qu1 ● David A. Hutchins 1 Received: 29 March 2019 / Revised: 4 September 2019 / Accepted: 13 September 2019 © The Author(s), under exclusive licence to International Society for Microbial Ecology 2019 Abstract Average sea surface temperatures are expected to rise 4° this century, and marine phytoplankton and bacterial community composition, biogeochemical rates, and trophic interactions are all expected to change in a future warmer ocean. Thermal experiments typically use constant temperatures; however, weather and hydrography cause marine temperatures to fluctuate on diel cycles and over multiple days. We incubated natural communities of phytoplankton collected from California coastal waters during spring, summer, and fall under present-day and future mean temperatures, using thermal treatments that were either constant or fluctuated on a 48 h cycle. As assayed by marker-gene sequencing, the emergent microbial communities were consistent within each season, except when culture temperatures exceeded the highest temperature recorded in a 10- year local thermal dataset. When temperature treatments exceeded the 10-year maximum the phytoplankton community shifted, becoming dominated by diatom amplicon sequence variants (ASVs) not seen at lower temperatures. When mean temperatures were above the 10-year maximum, constant and fluctuating regimes each selected for different ASVs. These findings suggest coastal microbial communities are largely adapted to the current range of temperatures they experience. They also suggest a general hypothesis whereby multiyear upper temperature limits may represent thresholds, beyond which large community restructurings may occur. Now inevitable future temperature increases that exceed these environmental thresholds, even temporarily, may fundamentally reshape marine microbial communities and therefore the biogeochemical cycles that they mediate. Introduction Marine phytoplankton draw down atmospheric CO2, support marine food webs, and provide long-term carbon storage in underlying deep waters [1]. Currently, anthropogenic CO2 inputs are inducing changes in phytoplankton communities by changing temperature and climate regimes [2]. Present-day atmospheric CO2 con-centrations of >400 ppm have not been seen for almost 12 million years, and these past elevated CO2 events were accompanied by substantial warming [3, 4]. The high specific heat of seawater has meant that warming of the ocean’s surface has happened more slowly than warming of land. Even so, global mean sea surface temperature (SST) has gone up 0.7 °C in the last three decades, and is expected to rise an additional 4 °C this century [3, 5, 6]. Warming influences phytoplankton growth and physiol-ogy [7, 8]. Growth rates across temperatures for phyto-plankton typically have thermal performance curves (TPC) that increase gradually with rising temperatures to an opti-mal maximum, then decrease rapidly at higher temperatures [9]. Thermal optima and limits for species are typically connected to in situ thermal regimes. For instance, phyto-plankton at lower latitudes often live near their optimal temperatures, whereas temperate species are temperature-limited [10–12]. Because of the rapid decrease in growth * David A. Hutchins dahutch@usc.edu 1 Department of Biological Sciences, University of Southern California, Los Angeles, CA 90007, USA 2 Exobiology Branch, NASA Ames Research Center, Moffett Blvd., Mountain View, CA 94035, USA 3 School of Life Sciences, Xiamen University, 361005 Xiamen, China Supplementary information The online version of this article (https:// doi.org/10.1038/s41396-019-0525-6) contains supplementary material, which is available to authorized users. 1234567890();,: 1234567890();,: |
