DOCSLIB.ORG

Autotrophic and Heterotrophic Acquisition of Carbon and Nitrogen by a Mixotrophic Chrysophyte Established Through Stable Isotope Analysis

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Autotrophic and Heterotrophic Acquisition of Carbon and Nitrogen by a Mixotrophic Chrysophyte Established Through Stable Isotope Analysis OPEN The ISME Journal (2017) 11, 2022–2034 www.nature.com/ismej ORIGINAL ARTICLE Autotrophic and heterotrophic acquisition of carbon and nitrogen by a mixotrophic chrysophyte established through stable isotope analysis Ramon Terrado1, Alexis L Pasulka2, Alle A-Y Lie1, Victoria J Orphan2, Karla B Heidelberg1 and David A Caron1 1Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA and 2Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, USA Collectively, phagotrophic algae (mixotrophs) form a functional continuum of nutritional modes between autotrophy and heterotrophy, but the specific physiological benefits of mixotrophic nutrition differ among taxa. Ochromonas spp. are ubiquitous chrysophytes that exhibit high nutritional flexibility, although most species generally fall towards the heterotrophic end of the mixotrophy spectrum. We assessed the sources of carbon and nitrogen in Ochromonas sp. strain BG-1 growing mixotrophically via short-term stable isotope probing. An axenic culture was grown in the presence of either heat-killed bacteria enriched with 15N and 13C, or unlabeled heat-killed bacteria and labeled inorganic substrates (13C-bicarbonate and 15N-ammonium). The alga exhibited high growth rates (up to 2 divisions per day) only until heat-killed bacteria were depleted. NanoSIMS and bulk IRMS isotope analyses revealed that Ochromonas obtained 84–99% of its carbon and 88–95% of its nitrogen from consumed bacteria. The chrysophyte assimilated inorganic 13C-carbon and 15N-nitrogen when bacterial abundances were very low, but autotrophic (photosynthetic) activity was insufficient to support net population growth of the alga. Our use of nanoSIMS represents its first application towards the study of a mixotrophic alga, enabling a better understanding and quantitative assessment of carbon and nutrient acquisition by this species. The ISME Journal (2017) 11, 2022–2034; doi:10.1038/ismej.2017.68; published online 19 May 2017 Introduction behavior, is not widely acknowledged or understood. Some attempts have been made to classify mixo- Aquatic microbial food webs encompass interactions trophs in a few conceptual models (Våge et al., 2013; between bacteria, cyanobacteria, phototrophic and Andersen et al., 2015; Mitra et al., 2016; Ward and heterotrophic protists, and viruses (Azam and Follows, 2016), but the importance of mixotrophic Malfatti, 2007; Sarmento, 2012; Worden et al., organisms to food web structure and function has not 2015). Models of these food webs generally char- yet routinely been entrained into mathematical acterize eukaryotic microbes as either phototrophic models of food web dynamics. (capable of producing energy and fixing carbon for Mixotrophic species exhibit a range of nutritional growth using only inorganic compounds and light) behaviors. Some species are predominantly photo- or heterotrophic (dependent on the consumption of trophic but supplement photosynthesis with a small organic material for nutrition). These characteriza- amount of heterotrophy, while other species are tions greatly oversimplify trophic interactions predominantly heterotrophic and use photosynthesis because many microbial eukaryotic algae are mixo- only for extending survival when prey are scarce trophic, capable of using both inorganic and organic forms of carbon and major nutrients (Flynn et al., (Jones, 1994, 2000; Rottberger et al., 2013). Mixed 2013). Although the mixotrophic nature of many nutrition appears to provide an advantage particularly algae is now recognized, the impact of this behavior in oligotrophic ecosystems (Hartmann et al., 2012; in terms of carbon and nutrient cycling, as well as its Unrein et al., 2014), presumably because nutrients are ecological significance for the algae that conduct this often limiting to purely phototrophic protists, while strict heterotrophs are limited by prey availability. In contrast, mixotrophic protists may meet their elemen- Correspondence: DA Caron, Department of Biological Sciences, tal and energy demands through a mixture of photo- University of Southern California, 3616 Trousdale Ave., AHF 301, synthesis and prey ingestion. Yet, mixotrophic algae Los Angeles, CA, 90089-0371, USA. E-mail: [email protected] do not dominate all ecosystems, and therefore mixed Received 21 October 2016; revised 20 March 2017; accepted nutrition appears to impose tradeoffs that are not well 3 April 2017; published online 19 May 2017 understood (Raven, 1997; Stoecker, 1998). Mixotrophy by a chrysophyte alga R Terrado et al 2023 More than 100 mixotrophic species of Chrysophy- bacterial prey (Sanders et al., 2001), we hypothesize ceae have been described, and sequence-based that this Ochromonas strain, in the presence of high surveys of natural samples point to potentially larger bacterial abundances, would acquire an elevated diversity (Andersen, 2007; del Campo and Massana, percentage of its carbon and nitrogen requirements 2011). The group presents interesting model species through heterotrophy via the ingestion and assimila- for investigating mixotrophy due to the wide tion of bacteria. Our analysis showed that while diversity of nutritional strategies among these spe- defined as a mixotroph, this strain of Ochromonas cies. Some, such as Uroglena americana, appear to relies primarily on bacterial phagotrophy for both be primarily autotrophic but require a phospholipid carbon and nitrogen acquisition and that photo- that is obtained via phagocytosis of prey (Kimura synthesis remains a minor aspect of its nutrition. and Ishida, 1989). A similar case has been reported for Dinobryon cylindricum, where phagocytosis might also provide essential growth factors and/or Materials and methods nutrients for photosynthetic growth (Caron et al., Bacterial isolation and production of heat-killed 1993). At the other end of the spectrum, species exist bacteria that exhibit primarily heterotrophic metabolism Heat-killed bacteria (HKB) were prepared as non- where phototrophy appears to be of minor signifi- living prey for all experimental work in this study to cance (Andersson et al., 1989; Caron et al., 1990; avoid uptake or release of organic or inorganic Boraas et al., 1992; Sanders et al., 2001; Foster and substances by bacteria in the axenic culture of the Chrzanowski, 2012; Chrzanowski and Foster, 2014; chrysophyte. Bacteria from a bacterized culture of Wilken et al., 2014). Ochromonas BG-1 were streaked on petri dishes Experiments with mixotrophic algae have yielded with a solid agar medium containing a minimal M9 results that outline the overall metabolism of these medium (Marley et al., 2001) using ammonium as organisms (Sanders and Porter, 1988; Sanders, 2011), the sole source of nitrogen and glucose as the sole but most studies have not clearly defined the sources source of carbon. Individual colonies were trans- (phototrophy or heterotrophy) of carbon and nutri- ferred to 25 ml tubes containing the M9 medium ents in these species. Similarly, recent molecular (without agar), which were used to inoculate 1.5 l of studies offer insights into the metabolic potential of medium and incubated at 20 °C on a shaker table in these algae (Liu et al., 2015; Terrado et al., 2015; Liu order to obtain large numbers of bacteria for the et al., 2016), but do not specifically quantify the production of HKB. Cultures were grown to station- contributions of photosynthesis and heterotrophy to ary phase, and cells were transferred into 200 ml mixotrophic nutrition. Stable isotope probing (SIP) bottles and heat-killed in a water bath at 70 °C for at offers a method to address this issue. Combining SIP least 1 h. Cells were transferred into 50 ml sterile with high-resolution nanometer-scale secondary ion Falcon tubes and concentrated by centrifugation mass spectrometry (nanoSIMS), researchers have using an Allegra 25 R centrifuge (Beckman Coulter, been able to quantify and map elemental and Inc., Brea, CA, USA) equipped with a TS-5.1-500 – isotopic abundances at 50 100 nm resolution in swinging bucket rotor (Beckman Coulter) at 5000 r.p. order to assess the metabolic activities and elemental m for 15 min. Supernatant was discarded and cells flow within individual cells (Boxer et al., 2009; Gao re-suspended using sterile Milli-Q water by vortex- et al., 2016). The approach has been used to ing. Cells were centrifuged and washed at least three characterize the metabolic potential and anabolic times. After the final wash, cells were re-suspended activity in environmental microorganisms (Orphan in sterile Milli-Q water, and aliquots were stored and House, 2009; Orphan, 2009), including the frozen in 2 ml Eppendorf tubes until use. The utilization of different carbon substrates by deep effectiveness of the heat-killing process was verified sub-seafloor bacterial cells (Morono et al., 2011), by inoculating aliquots of the HKB into rich nutrient carbon and nitrogen utilization by cyanobacteria broth and monitoring for growth. (Popa et al., 2007; Finzi-Hart et al., 2009), the flux of In order to label bacteria with stable isotopes, the nitrogen within coral symbionts (Kopp et al., 2013), glucose and ammonium in the M9 medium were the transfer of nitrogen from lysed algae to bacteria substituted with D-glucose-1-13C (glucose 4% final (Sheik et al., 2014) and the transfer of carbon to concentration, 99 atom % 13C, Sigma-Aldrich Corp., bacterial surface symbionts of a large cellulolytic St Louis, MO, USA) and ammonium-15N chloride protist symbiont of a
Load more

Recommended publications
  • Destabilization, Stabilization, and Multiple Attractors in Saturated Mixotrophic Environments
    Downloaded from orbit.dtu.dk on: Sep 27, 2021 Destabilization, stabilization, and multiple attractors in saturated mixotrophic environments Lindstrom, Torsten; Cheng, Yuanji; Chakraborty, Subhendu Published in: SIAM Journal on Applied Mathematics Link to article, DOI: 10.1137/19M1294186 Publication date: 2020 Document Version Publisher's PDF, also known as Version of record Link back to DTU Orbit Citation (APA): Lindstrom, T., Cheng, Y., & Chakraborty, S. (2020). Destabilization, stabilization, and multiple attractors in saturated mixotrophic environments. SIAM Journal on Applied Mathematics, 80(6), 2338-2364. https://doi.org/10.1137/19M1294186 General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. Users may download and print one copy of any publication from the public portal for the purpose of private study or research. You may not further distribute the material or use it for any profit-making activity or commercial gain You may freely distribute the URL identifying the publication in the public portal If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. SIAM J. APPL.MATH. © 2020 Society for Industrial and Applied Mathematics Vol. 80, No. 6, pp. 2338{2364 DESTABILIZATION, STABILIZATION, AND MULTIPLE ATTRACTORS IN SATURATED MIXOTROPHIC ENVIRONMENTS\ast \" y z x TORSTEN LINDSTROM , YUANJI CHENG , AND SUBHENDU CHAKRABORTY Abstract. The ability of mixotrophs to combine phototrophy and phagotrophy is now well recognized and found to have important implications for ecosystem dynamics.
    [Show full text]
  • Bioenergetics of Mixotrophic Metabolisms: a Theoretical Analysis
    Bioenergetics of mixotrophic metabolisms: A theoretical analysis by Stephanie Slowinski A thesis presented to the University of Waterloo in fulfillment of the thesis requirement for the degree of Master of Science in Earth Sciences (Water) Waterloo, Ontario, Canada, 2019 © Stephanie Slowinski 2019 Author’s Declaration This thesis consists of material all of which I authored or co-authored: see Statement of Contributions included in the thesis. This is a true copy of the thesis, including any required final revisions, as accepted by my examiners. I understand that my thesis may be made electronically available to the public. ii Statement of Contributions This thesis consists of two co-authored chapters. I contributed to the study design and execution in chapters 2 and 3. Christina M. Smeaton (CMS) and Philippe Van Cappellen (PVC) provided guidance during the study design and analysis. I co-authored both of these chapters with CMS and PVC. iii Abstract Many biogeochemical reactions controlling surface water and groundwater quality, as well as greenhouse gas emissions and carbon turnover rates, are catalyzed by microorganisms. Representing the thermodynamic (or bioenergetic) constraints on the reduction-oxidation reactions carried out by microorganisms in the subsurface is essential to understand and predict how microbial activity affects the environmental fate and transport of chemicals. While organic compounds are often considered to be the primary electron donors (EDs) in the subsurface, many microorganisms use inorganic EDs and are capable of autotrophic carbon fixation. Furthermore, many microorganisms and communities are likely capable of mixotrophy, switching between heterotrophic and autotrophic metabolisms according to the environmental conditions and energetic substrates available to them.
    [Show full text]
  • Worksheet Class 7Th ( Science ) Chapter 1St Nutrition in Plants
    Worksheet Class 7th ( science ) Chapter 1st Nutrition in plants 1. Autotrophic nutrition 2. Heterotrophic Nutrition The mode of nutrition in which organisms obtain their food from others ( plants and animals ) is called heterotrophic nutrition. Heterotrophs :- Organisms that are not capable of synthesising their own food and depend on other organisms for their food requirements are called heterotrophs. They are also called consumers. Heterotrophic Nutrition in plants Heterotrophic nutrition in non-green plants are of three types- (i) Saprotrophic (ii) Parasitic (iii) Symbiotic (I) Saprotrophic nutrition The mode of nutrition in which organisms take in nutrients from dead and decaying matter is called saprotrophic nutrition. Saprotrophs or saprophytes Saprotrophs are the organisms that feed on dead and decaying matter. Example :- Fungi, mushrooms Saprophytes are also called cleaners of the environment. (II) Parasitic Nutrition The mode of nutrition in which an organism lives on or inside the body of other living organism (host) is called parasitic nutrition. Parasitic plants are of two types • Total parasites • Partial parasites Total parasites These plants cannot make their own food and derive all of it from the host plant. E.g.- cuscuta (amarbel) is total stem parasite and Rafflesia is total root parasite plant. Partial parasites They have green leaves, therefore can make their food for themselves. However, they get water and minerals from host plant. E.g.- mistletoe is a partial stem parasite and sandalwood is a partial root parasite. (III) Symbiotic Nutrition Symbionts:- Two organisms living in close physical contact with each other and providing mutual benefits are called symbionts. Symbiosis:- Condition of living together is called symbiosis.
    [Show full text]
  • Biophysical Aspects of Resource Acquisition and Competition in Algal Mixotrophs
    vol. 178, no. 1 the american naturalist july 2011 Biophysical Aspects of Resource Acquisition and Competition in Algal Mixotrophs Ben A. Ward,* Stephanie Dutkiewicz, Andrew D. Barton, and Michael J. Follows Department of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139 Submitted November 10, 2010; Accepted March 15, 2011; Electronically published June 6, 2011 polar waters, for example, mixotrophy provides dinofla- abstract: Mixotrophic organisms combine autotrophic and het- gellates with the flexibility to endure large environmental erotrophic nutrition and are abundant in both freshwater and marine environments. Recent observations indicate that mixotrophs consti- changes during tidal and seasonal cycles (Li et al. 2000; tute a large fraction of the biomass, bacterivory, and primary pro- Litchman 2007). However, in the low-seasonality sub- duction in oligotrophic environments. While mixotrophy allows tropical oceans, where such nonequilibrium dynamics are greater flexibility in terms of resource acquisition, any advantage presumably much less important, mixotrophy remains a must be traded off against an associated increase in metabolic costs, prevalent strategy. Zubkov and Tarran (2008) recently which appear to make mixotrophs uncompetitive relative to obligate found that photosynthetic protist species, which account autotrophs and heterotrophs. Using an idealized model of cell phys- iology and community competition, we identify one mechanism by for more than 80% of the total chlorophyll in regions of which mixotrophs can effectively outcompete specialists for nutrient the North Atlantic, were also responsible for 40%–95% of elements. At low resource concentrations, when the uptake of nu- the total bacterivory. Small mixotrophs have been shown trients is limited by diffusion toward the cell, the investment in cell to be of similar importance in coastal oligotrophic waters membrane transporters can be minimized.
    [Show full text]
  • Nutritional and Reproductive Strategies in a Chemosymbiotic Bivalve Living in a Tropical Intertidal Seagrass Bed
    Vol. 501: 113-126, 2014 MARINE ECOLOGY PROGRESS SERIES Published March 31 doi: 10.3354/mepsl0702 Mar Ecol Prog Ser OPEN ACCESS © ® Nutritional and reproductive strategies in a chemosymbiotic bivalve living in a tropical intertidal seagrass bed Matthijs van der Geest1*, Amadou Abderahmane Sail2, Sidi Ould Ely3, Reindert W. Nauta1, Jan. A. van Gils1, Theunis Piersma1,4 1NIOZ Royal Netherlands Institute for Sea Research, PO Box 59, 1790 AB Den Burg, Texel, The Netherlands 2Mauritanian Institute for Oceanographic Research and Fisheries (IMROP), BP 22, Nouadhibou, Mauritania 3Parc National du Banc d'Arguin, BP 5355, Nouakchott, Mauritania 4Chair in Global Flyway Ecology, Animal Ecology Group, Centre for Ecological and Evolutionary Studies (CEES), University of Groningen, PO Box 11103, 9700 CC Groningen, The Netherlands ABSTRACT: Sulphide-oxidizing endosymbiont-bearing bivalves often dominate the infauna of seagrass-covered sediments, where they control sulphide levels and contribute to carbon cycling by feeding on chemosynthetically fixed carbon and suspended particulate organic matter (SPOM). Previous studies from temperate habitats suggest that SPOM availability may regulate growth and reproduction, since SPOM may be of greater nutritional value than the material provided by bacterial endosymbionts. To examine if changes in diet correlate with body condition and repro­ ductive activity, we studied seasonal patterns in somatic and gonadal investment and gameto- genic development in relation to nutrition in the endosymbiont-bearing bivalveLoripes lucinalis in seagrass-covered intertidal flats at a tropical study site (Banc d'Arguin, Mauritania). Carbon stable isotope analysis revealed clear seasonal cycles in the relative heterotrophic contribution to the diet of Loripes, with mean monthly values ranging from 21% in March to 39% in September.
    [Show full text]
  • An Improved Model of Carbon and Nutrient Dynamics in the Microbial Food Web in Marine Enclosures
    AQUATIC MICROBIAL ECOLOGY Vol. 14: 91-108.1998 Published January 2 Aquat Microb Ecol An improved model of carbon and nutrient dynamics in the microbial food web in marine enclosures 'Ecological Modelling Centre, Joint Department of Danish Hydraulic Institute and VKI, Agern Alle 5, DK-2970 Harsholrn, Denmark 'VKI, Agern All6 11, DK-2970 Harsholrn, Denmark 3National Environmental Research Institute, PO Box 358, Frederiksborgvej 399, DK-4000 Roskilde, Denmark ABSTRACT: A description of an improved dynamic simulation model of a marine enclosure 1s given. New features In the model are the inclusion of picoalgae and rnixotrophs; the ability of bacteria to take up dissolved inorganic nutrients directly; and, for the phytoplankton functional groups, the inclusion of luxury uptake and the decoupling of the nutrient uptake dynamics from carbon-assimilat~ondynamics. This last feature implies dynamically variable phosphorus/carbon and nitrogedcarbon ratios. The model was calibrated with experimental results from enclosure experiments carried out in Knebel Vig, a shallow microtidal land-locked fjord in Denmark, and verified with results from enclosure experi- ments in Hylsfjord, a deep and salinity-stratified Norwegian fjord. Both observations and model simu- lation~showed dominance of a microbial food web in control enclosures with low productivity. In N- and P-enriched enclosures a classical food web developed, while an intermediate system was found in N-, P- and Si-enriched enclosures. Mixotrophic flagellates were most important in the nutrient-limited control enclosures where they accounted for 49% of the pigmented biomass and about 48% of the primary production. Lumping the mixotrophs in the simulation model with either the autotrophic or the heterotrophic functional groups reduced total primary production by 74 %.
    [Show full text]
  • Hetrotrophic-Nutrition-O-Level.Pdf
    Heterotrophic nutrition Heterotrophic organisms are organisms that feed on complex ready-made organic food. They use it as source of: - (i) energy for their vital activities, (ii) building materials, that is specific atoms and molecules for cell maintenance and repair and growth, (iii) vitamins (co-enzymes) that cannot be synthesised in organism but which are vital specific cellular processes. The main forms of heterotrophic nutrition include (i) holozoic, (ii) saprotrophic (or saprophytic) e.g. mould, mushroom (iii) mutualistic (iv) parasitic, although some overlap between groups may occur. Holozoic nutrition It is a type of heterotrophic nutrition involves the following processes (i) Ingestion: is taking in of complex organic food(solid or liquid). (ii) Digestion: is the breakdown of large complex insoluble organic molecules into small, simple soluble diffusible molecules. This is achieved by mechanical break down and enzymatic hydrolysis. Digestion may be either extra or intra cellular. (iii)Absorption: is the uptake of the soluble molecules from the digestion region, across a membrane and into the body tissue proper. The food may pass into the blood stream to be transported to appropriate regions within the body of the organism. (iv) Assimilation is the utilisation of the absorbed molecules by the body to provide either energy or materials to be incorporated into the body. (v) Egestion is the elimination from the body of undigested waste food materials. Animals which feed one plants are called herbivores, those that feed on other animals carnivores, and those that eat a mixed diet of animal and vegetable matter are termed omnivores. If they take in food in form of small particles the animals are microphagous feeders, for example earthworms, whereas if the food is ingested in liquid form they are, classed as fluid feeders, such as aphids and mosquitoes.
    [Show full text]
  • Class - 7 Subject - SCIENCE Chapter - 1 FOOD A
    BIJENDRA PUBLIC SCHOOL Class - 7 Subject - SCIENCE Chapter - 1 FOOD A. Very Short Answer Questions : (Answer in one word) 1. Name the process by which green plants make their food. Ans. Photosynthesis 2. What type of heterotroph is a frog? Ans. Carnivore 3. What are the small pores on the under surface of the leaves called? Ans. Stomata 4. What is the mode of nutrition in fungi? Ans. Saprophytic 5. Where does the bacterium Rhizobium live? Ans. Root nodules in a legume. B. Short - Answer Questions : Answer in 10-15 words. 1. Why are the animals and human called heterotrophs? Ans. The organisms that cannot make their own food are called heterotrophs. Since animals and humans cannot make their own food, so they are called heterotrophs. 2. Name the factors which affect photosynthesis. Ans. The factors that affect photosynthesis are light intensity, nature of light, availability of carbon dioxide and water and temperature. 3. Name one each of a. totally parasitic b. partial parasitic plants. Ans. a. Total parasitic plant: Cuscuta (Amarbel) and Apodauthes b. Partial parasitic plants: Mistletoe 4. How are the soil nutrients replenished? Ans. Nutrients in the soil can be replenished by one or more of the following methods. * By using manure * By using fertilizers * By adopting crop-rotation method 5. What is crop-rotation method? Ans. In crop-rotaion method a cereal crop is sown alternately to a leguminous crop. This is done to replenish the nutrients (specially nitrogen) in the soil. C. Long Answer Type Questions (Answer in 20-25 words) 1. What are the functions of food? Ans.
    [Show full text]
  • 22. Life Processes
    MODULE - 5 Life Processes-1 Nutrition, Transportation, Respiration and Excretion The Living World 22 Notes LIFE PROCESSES-1 NURTRITION, TRANSPORTATION, RESPIRATION AND EXCRETION The activities by which living organisms take in food, derive energy, remove waste from their body and respond to changes in the environment are called life processes. In this lesson, you will learn about basic life processes, namely nutrition, respiration, transportation of nutrients and fluids in the body, and excretion. OBJECTIVES After completing this lesson, you will be able to: • emphasize the need for energy requirement for life processes; • explain the steps in photosynthesis; • appreciate the various modes of heterotrophic nutrition in living organisms; • realize the importance of the process of nutrition in humans,identify nutritional disorders and explain the concept of balanced diet; • outline the need for and steps in the process of respiration; • explain the fundamental aspects of transport of material(food, waste etc.) in plants and animals (e.g. humans); • explain the process of excretion in humans. I. NUTRITION 22.1 WHY DO WE NEED FOOD How do you feel if you do not have food for a day or two? You may feel exhausted and weak. But if you do not get food for a few days, will you survive and grow? You will probably say‘No’. We know that living beings need food to survive. Food provides 58 SCIENCE AND TECHNOLOGY Life Processes-1 Nutrition, Transportation, Respiration and Excretion MODULE - 5 The Living World the essential raw material that our body needs to grow and stay healthy. It also provides energy to carry out various life processes.
    [Show full text]
  • MIXOTROPHY in FRESHWATER FOOD WEBS a Dissertation
    MIXOTROPHY IN FRESHWATER FOOD WEBS A Dissertation Submitted to the Temple University Graduate Board In Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY by Sarah B. DeVaul May 2016 Examining Committee Members: Robert W. Sanders, Advisory Chair, Biology Erik E. Cordes, Biology Amy Freestone, Biology Dale Holen, External Member, Penn State Worthington Scranton © Copyright 2016 by Sarah B. DeVaul All Rights Reserved ii ABSTRACT Environmental heterogeneity in both space and time has significant repercussions for community structure and ecosystem processes. Dimictic lakes provide examples of vertically structured ecosystems that oscillate between stable and mixed thermal layers on a seasonal basis. Vertical patterns in abiotic conditions vary during both states, but with differing degrees of variation. For example, during summer thermal stratification there is high spatial heterogeneity in temperature, nutrients, dissolved oxygen and photosynthetically active radiation. The breakdown of stratification and subsequent mixing of the water column in fall greatly reduces the stability of the water column to a vertical gradient in light. Nutrients and biomass that were otherwise constrained to the depths are also suspended, leading to a boom in productivity. Freshwater lakes are teeming with microbial diversity that responds to the dynamic environment in a seemingly predictable manner. Although such patterns have been well studied for nanoplanktonic phototrophic and heterotrophic populations, less work has been done to integrate the influence of mixotrophic nutrition to the protistan assemblage. Phagotrophy by phytoplankton increases the complexity of nutrient and energy flow due to their dual functioning as producers and consumers. The role of mixotrophs in freshwater planktonic communities also varies depending on the relative balance between taxon-specific utilization of carbon and energy sources that ranges widely between phototrophy and heterotrophy.
    [Show full text]
  • Mixotrophy in Planktonic Communities Title: Intraguild Predation Enables
    Running Head: Mixotrophy in planktonic communities Title: Intraguild predation enables coexistence of competing phytoplankton in a well-mixed water column Authors: Holly V. Moeller1,2,3,∗, Michael G. Neubert1, and Matthew D. Johnson1 1. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA; 2. Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada. 3. Current Address: Department of Ecology, Evolution, & Marine Biology, University of Califor- nia, Santa Barbara, Santa Barbara, California 93106, USA; ∗ Corresponding author; email: [email protected] Manuscript elements: 5 figures, 1 table, online appendix A (including figures A1-9). Figures 1, 4, 5, and A1-A3 are in color. Manuscript type: Article 1 Abstract: Resource competition theory predicts that when two species compete for a single, finite resource, 3 the better competitor should exclude the other. However, in some cases, weaker competitors can persist through intraguild predation, i.e., by eating their stronger competitor. Mixotrophs, species that meet their carbon demand by combining photosynthesis and phagotrophic heterotro- 6 phy, may function as intraguild predators when they consume the phototrophs with which they compete for light. Thus, theory predicts that mixotrophy may allow for coexistence of two species on a single limiting resource. We tested this prediction by developing a new mathematical model 9 for a unicellular mixotroph and phytoplankter that compete for light, and comparing the model’s predictions with a laboratory experimental system. We find that, like other intraguild predators, mixotrophs can persist when an ecosystem is sufficiently productive (i.e., the supply of the lim- 12 iting resource, light, is relatively high), or when species interactions are strong (i.e., attack rates and conversion efficiencies are high).
    [Show full text]
  • Microbial Sulfur Transformations in Sediments from Subglacial Lake Whillans
    ORIGINAL RESEARCH ARTICLE published: 19 November 2014 doi: 10.3389/fmicb.2014.00594 Microbial sulfur transformations in sediments from Subglacial Lake Whillans Alicia M. Purcell 1, Jill A. Mikucki 1*, Amanda M. Achberger 2 , Irina A. Alekhina 3 , Carlo Barbante 4 , Brent C. Christner 2 , Dhritiman Ghosh1, Alexander B. Michaud 5 , Andrew C. Mitchell 6 , John C. Priscu 5 , Reed Scherer 7 , Mark L. Skidmore8 , Trista J. Vick-Majors 5 and the WISSARD Science Team 1 Department of Microbiology, University of Tennessee, Knoxville, TN, USA 2 Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, USA 3 Climate and Environmental Research Laboratory, Arctic and Antarctic Research Institute, St. Petersburg, Russia 4 Institute for the Dynamics of Environmental Processes – Consiglio Nazionale delle Ricerche and Department of Environmental Sciences, Informatics and Statistics, Ca’ Foscari University of Venice, Venice, Italy 5 Department of Land Resources and Environmental Sciences, Montana State University, Bozeman, MT, USA 6 Geography and Earth Sciences, Aberystwyth University, Ceredigion, UK 7 Department of Geological and Environmental Sciences, Northern Illinois University, DeKalb, IL, USA 8 Department of Earth Sciences, Montana State University, Bozeman, MT, USA Edited by: Diverse microbial assemblages inhabit subglacial aquatic environments.While few of these Andreas Teske, University of North environments have been sampled, data reveal that subglacial organisms gain energy for Carolina at Chapel Hill, USA growth from reduced minerals containing nitrogen, iron, and sulfur. Here we investigate Reviewed by: the role of microbially mediated sulfur transformations in sediments from Subglacial Aharon Oren, The Hebrew University of Jerusalem, Israel Lake Whillans (SLW), Antarctica, by examining key genes involved in dissimilatory sulfur John B.
    [Show full text]