On the response of marine phytoplankton to changing nutrient and light conditions [electronic resource]

Marine phytoplankton are photoautotrophic microorganisms that synthesize organic biomass from mineral nutrients and form the base of the marine food web. Marine phytoplankton are increasingly being recognized as important contributors to biogeochemical cycling of chemical elements, including carbon (C), and therefore play a role in controlling Earth's climate. A relatively recent estimate suggests that while the upper 100 meters of the ocean contains less than 1 percent of the total global photosynthetic biomass, this small fraction of the marine environment accounts for nearly 50 percent of global primary production, the process by which atmospheric carbon dioxide is incorporated into biomass through photosynthesis. Nutrients and light affect phytoplankton growth, and their availability exerts considerable control on phytoplankton distributions in the ocean and their contribution to biogeochemical cycles. The global supply, distribution, and availability of nutrients in the ocean are driven by a range of physical and biological factors. However, light availability is determined primarily by attenuation within the water column. The ability of a phytoplankton group to respond to changes in nutrient and light availability ultimately determines whether that group will persist, or whether community succession will permit different, more ecologically competitive groups to prevail. The overarching goal of this dissertation is to identify and understand how responses to changing resource availability influence the competitive success of phytoplankton, and to increase our understanding of how phytoplankton affect biogeochemical cycling of C and other important nutrients in the ocean. The dissertation includes an Introduction (Chapter 1), and seven research chapters (Chapters 2-8) covering separate bodies of work, each focusing on a different topic as outlined below. In Chapter 1, general background information is provided about nutrient and light regimes in the ocean, and about the basic biology and ecology of phytoplankton. Chapter 2 (entitled: The phosphorus cycle) provides an overview of the phosphorus (P) cycle including sources, sinks, and transport pathways of P in the environment, microbially-mediated processes and their genetic regulation, methods for assessing environmental P concentrations and microbial phosphate status, and a discussion of microbial responses to anthropogenic changes to the P cycle. This chapter was published in 2009 in The Encyclopedia of Microbiology, 3rd Edition, edited by Moselio Schaechter, Elsevier. Chapter 3 is entitled: Phosphorus availability, phytoplankton community dynamics, and taxon-specific phosphorus status in the Gulf of Aqaba, Red Sea. The study uses a novel cell stain to show that (1) coexisting groups of phytoplankton exposed to identical phosphate levels may have a different phosphate status, and (2) although increased alkaline phosphatase activity can serve as an indicator of phosphate limitation, it does not necessarily confer a competitive advantage to cells in oligotrophic waters, where smaller cell size may provide a more important competitive edge. The affinity of individual groups of phytoplankton for P may help determine community composition and lead to seasonal community succession as P availability changes dramatically throughout the year. This chapter was published in 2007 in Limnology and Oceanography 52: 873-885. Chapter 4 is entitled: Nitrogen cycling in oligotrophic waters: the influence of light and substrate availability. This study demonstrates that two major processes contribute to formation of nitrite maxima in the Gulf of Aqaba: (i) spatially segregated microbial oxidation of ammonium and nitrite during nitrification; and (ii) incomplete nitrate reduction to ammonium by light-limited phytoplankton. Field data and stable isotope (N-15) tracer experiments show that physical and biological characteristics of the water column determine which of the two nitrite formation processes becomes dominant at a given season and depth. Rates are reported for major N transformation reactions occurring in the N cycle. This chapter is currently in review with Limnology and Oceanography. Chapter 5 is entitled: Picophytoplankton responses to changing nutrient and light regimes during a bloom. In the Red Sea, the spring bloom is characterized by a rapid increase in photosynthetic biomass. Nutrient addition experiments and in situ monitoring show that picoeukaryotes and Synechococcus have a bloomer growth strategy, have higher P requirements relative to N, and are responsible for the majority of photosynthetic biomass in surface waters. In contrast, light limited populations show rapid photoacclimation and community shifts following stratification. The traditional interpretation of "bloom" dynamics (i.e. increase in biomass) may therefore be confined to surface waters where light is not limiting, while other acclimation processes are more ecologically relevant at depth. This chapter was published in 2009 in Marine Biology 156: 1531-1546. Chapter 6 is entitled: A photosynthetic strategy for coping in a high light, low nutrient environment. This chapter reports field observations from the Atlantic and Pacific Oceans that show the reduction of oxygen is important for preserving photosynthetic efficiency in oligotrophic waters where low Fe levels may limit PSI and cytochrome b6f biogenesis. Despite midday photoinhibition (depression in the maximum photochemical yield, Fv/Fm), cells do not show a decreased capacity for carbon dioxide fixation. Instead, the fraction of oxidized functional PSII reaction centers increases at midday, counteracting the loss of functional centers stemming from photoinhibition. This process was not apparent in the coastal phytoplankton populations monitored in this study, and may be a strategy unique to open ocean phytoplankton. This chapter was published in 2008 in Limnology and Oceanography 53: 900-913. Chapter 7 is entitled: The influence of atmospheric nutrients on primary productivity in a coastal upwelling region. This chapter is the first study to quantify the role of atmospheric deposition in supporting productivity an upwelling-dominated system (coastal California). Soluble nutrient measurements from locally-collected aerosols, oceanographic and atmospheric data from long-term monitoring programs and the MODIS satellite record, and laboratory culture experiments are used. The aerosol-Chlorophyll a relationship is significant in the summer, and is stronger at offshore locations than near the coast. Atmospheric nutrient sources are more important during El Niño periods when upwelling is suppressed, a phenomenon that may become more common due to climate warming. During high deposition non-upwelling periods aerosol N could support up to 20 percent of new production. Expanding our analysis to other regions, we find that atmospheric deposition may support up to 8 percent of production annually in other major coastal upwelling regions around the world. This chapter is currently in review with Global Biogeochemical Cycles. Chapter 8 is entitled: Toxicity of metals on marine Synechococcus. Atmospheric deposition of aerosols to the surface ocean is a source of nutrients for phytoplankton. However, this study demonstrates that atmospheric aerosols also contain components like copper (Cu), which are toxic to some phytoplankton above certain threshold levels. Incubations of natural phytoplankton assemblages with local aerosols show that metal toxicity can cause a major shift in phytoplankton community composition, suggesting that atmospheric aerosols may play a larger role in controlling phytoplankton species distributions than previously believed. Specific metal toxicity threshold concentrations were determined based on laboratory culture experiments with coastal and oceanic strains of Synechococcus, and oceanic strains are more susceptible to metal toxicity at lower concentrations and for a larger number of metals. A portion of this chapter was published as part of a larger study that also included a global model for Cu deposition in aerosols that was published in 2009 in The Proceedings of the National Academy of Science 106: 4601-4605 Chapter 9 discusses ideas for future work. The dissertation provides valuable information about how phytoplankton respond to resource availability in a number of different marine environments. The physical environment is shown to play an important role in determining nutrient and light availability over short term periods (e.g. transient exposure to high light during mixing, episodic delivery of aerosol nutrients) as well as over predictable seasonal cycles (e.g. deep convective mixing and stratification). Physiological acclimation of individual phytoplankton to these perturbations allows each species to survive over a broader range of conditions, increasing their competitive advantage. Similarly, succession allows the phytoplankton community as a whole to thrive over the broadest possible range of environmental conditions. This dissertation also shows that phytoplankton play an important role in the P and N cycles by generating organic substrates from inorganic substrates. In doing so, phytoplankton contribute substantially to primary production in coastal and open ocean habitats, and form and important link between the biotic and abiotic environment.

Advisor: Jacobson Mark Z. (Mark Zachary) primary advisor. Thesis advisor
Paytan Adina
Grossman Arthur (Arthur R.) advisor. Thesis advisor