Caron David A.

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Caron
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David A.
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Daily dynamics of contrasting spring algal blooms in Santa Monica Bay (central Southern California Bight)

2022-07-26 , Ollison, Gerid A. , Hu, Sarah K. , Hopper, Julie V. , Stewart, Brittany P. , Smith, Jayme , Beatty, Jennifer L. , Rink, Laura K. , Caron, David A.

Protistan algae (phytoplankton) dominate coastal upwelling ecosystems where they form massive blooms that support the world's most important fisheries and constitute an important sink for atmospheric CO2. Bloom initiation is well understood, but the biotic and abiotic forces that shape short-term dynamics in community composition are still poorly characterized. Here, high-frequency (daily) changes in relative abundance dynamics of the metabolically active protistan community were followed via expressed 18S V4 rRNA genes (RNA) throughout two algal blooms during the spring of 2018 and 2019 in Santa Monica Bay (central Southern California Bight). A diatom bloom formed after wind-driven, nutrient upwelling events in both years, but different taxa dominated each year. Whereas diatoms bloomed following elevated nutrients and declined after depletion each year, a massive dinoflagellate bloom manifested under relatively low inorganic nitrogen conditions following diatom bloom senescence in 2019 but not 2018. Network analysis revealed associations between diatoms and cercozoan putative parasitic taxa and syndinean parasites during 2019 that may have influenced the demise of the diatoms, and the transition to a dinoflagellate-dominated bloom.

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Preprint

Diversity and toxicity of Pseudo-nitzschia species in Monterey Bay : perspectives from targeted and adaptive sampling

2018-08 , Bowers, Holly A. , Ryan, John P. , Hayashi, Kendra , Woods, April , Marin, Roman , Smith, G. Jason , Hubbard, Katherine A. , Doucette, Gregory J. , Mikulski, Christina M. , Gellene, Alyssa G. , Zhang, Yanwu , Kudela, Raphael M. , Caron, David A. , Birch, James M. , Scholin, Christopher A.

Monterey Bay, California experiences near-annual blooms of Pseudo-nitzschia that can affect marine animal health and the economy, including impacts to tourism and commercial/recreational fisheries. One species in particular, P. australis, has been implicated in the most toxic of events, however other species within the genus can contribute to widespread variability in community structure and associated toxicity across years. Current monitoring methods are limited in their spatial coverage as well as their ability to capture the full suite of species present, thereby hindering understanding of HAB events and limiting predictive accuracy. An integrated deployment of multiple in situ platforms, some with autonomous adaptive sampling capabilities, occurred during two divergent bloom years in the bay, and uncovered detailed aspects of population and toxicity dynamics. A bloom in 2013 was characterized by spatial differences in Pseudo39 nitzschia populations, with the low-toxin producer P. fraudulenta dominating the inshore community and toxic P. australis dominating the offshore community. An exceptionally toxic bloom in 2015 developed as a diverse Pseudo-nitzschia community abruptly transitioned into a bloom of highly toxic P. australis within the time frame of a week. Increases in cell density and proliferation coincided with strong upwelling of nutrients. High toxicity was driven by silicate limitation of the dense bloom. This temporal shift in species composition mirrored the shift observed further north in the California Current System off Oregon and Washington. The broad scope of sampling and unique platform capabilities employed during these studies revealed important patterns in bloom formation and persistence for Pseudo-nitzschia. Results underscore the benefit of expanded biological observing capabilities and targeted sampling methods to capture more comprehensive spatial and temporal scales for studying and predicting future events.

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Preprint

Defining DNA-based operational taxonomic units for microbial-eukaryote ecology

2009-06-19 , Caron, David A. , Countway, Peter D. , Savai, Pratik , Gast, Rebecca J. , Schnetzer, Astrid , Moorthi, Stefanie D. , Dennett, Mark R. , Moran, Dawn M. , Jones, Adriane C.

DNA sequence information has been increasingly used in ecological research on microbial eukaryotes. Sequence-based approaches have included studies of the total diversity of selected ecosystems, the autecology of ecologically relevant species, and the identification and enumeration of species of interest to human health. It is still uncommon, however, to delineate protistan species based on their genetic signatures. The reluctance to assign species-level designations based on DNA sequences is partly a consequence of the limited amount of sequence information presently available for many free-living microbial eukaryotes, and partly the problematic nature and debate surrounding the microbial species concept. Despite the difficulties inherent in assigning species names to DNA sequences, there is a growing need to attach meaning to the burgeoning amount of sequence information entering the literature, and a growing desire to apply this information in ecological studies. We describe a computer-based tool that assigns DNA sequences from environmental databases to operational taxonomic units at approximate species-level distinctions. The approach provides a practical method for ecological studies of microbial eukaryotes (primarily protists) by enabling semiautomated analysis of large numbers of samples spanning great taxonomic breadth. Derivation of the algorithm was based on an analysis of complete small subunit ribosomal RNA (18S) gene sequences and partial gene sequences obtained from GenBank for morphologically described protistan species. The program was tested using environmental 18S data sets from two oceanic ecosystems. A total of 388 operational taxonomic units were observed among 2,207 sequences obtained from samples collected in the western North Atlantic and eastern North Pacific.

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Article

Defining planktonic protist functional groups on mechanisms for energy and nutrient acquisition : incorporation of diverse mixotrophic strategies

2016-01-03 , Mitra, Aditee , Flynn, Kevin J. , Tillmann, Urban , Raven, John A. , Caron, David A. , Stoecker, Diane K. , Not, Fabrice , Hansen, Per J. , Hallegraeff, Gustaaf M. , Sanders, Robert W. , Wilken, Susanne , McManus, George , Johnson, Matthew D. , Pitta, Paraskevi , Våge, Selina , Berge, Terje , Calbet, Albert , Thingstad, Frede , Jeong, Hae Jin , Burkholder, JoAnn M. , Glibert, Patricia M. , Graneli, Edna , Lundgren, Veronica

Arranging organisms into functional groups aids ecological research by grouping organisms (irrespective of phylogenetic origin) that interact with environmental factors in similar ways. Planktonic protists traditionally have been split between photoautotrophic “phytoplankton” and phagotrophic “microzooplankton”. However, there is a growing recognition of the importance of mixotrophy in euphotic aquatic systems, where many protists often combine photoautotrophic and phagotrophic modes of nutrition. Such organisms do not align with the traditional dichotomy of phytoplankton and microzooplankton. To reflect this understanding, we propose a new functional grouping of planktonic protists in an eco-physiological context: (i) phagoheterotrophs lacking phototrophic capacity, (ii) photoautotrophs lacking phagotrophic capacity, (iii) constitutive mixotrophs (CMs) as phagotrophs with an inherent capacity for phototrophy, and (iv) non-constitutive mixotrophs (NCMs) that acquire their phototrophic capacity by ingesting specific (SNCM) or general non-specific (GNCM) prey. For the first time, we incorporate these functional groups within a foodweb structure and show, using model outputs, that there is scope for significant changes in trophic dynamics depending on the protist functional type description. Accordingly, to better reflect the role of mixotrophy, we recommend that as important tools for explanatory and predictive research, aquatic food-web and biogeochemical models need to redefine the protist groups within their frameworks.

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Article

Mixotrophy : a widespread and important ecological strategy for planktonic and sea-ice nanoflagellates in the Ross Sea, Antarctica

2009-03-04 , Moorthi, Stefanie D. , Caron, David A. , Gast, Rebecca J. , Sanders, Robert W.

Mixotrophic nanoflagellates (MNF) were quantified in plankton and sea ice of the Ross Sea, Antarctica, during austral spring. Tracer experiments using fluorescently labeled bacteria (FLB) were conducted to enumerate MNF and determine their contribution to total chloroplastidic and total bacterivorous nanoflagellates. Absolute abundances of MNF were typically <200 ml–1 in plankton assemblages south of the Polar Front, but they comprised 8 to 42% and 3 to 25% of bacterivorous nanoflagellates in the water column and ice cores, respectively. Moreover, they represented up to 10% of all chloroplastidic nanoflagellates in the water column when the prymnesiophyte Phaeocystis antarctica was blooming (up to 23% if P. antarctica, which did not ingest FLB, was excluded from calculations). In ice cores, MNF comprised 5 to 10% of chloroplastidic nanoflagellates. The highest proportions of MNF were found in some surface water samples and in plankton assemblages beneath ice, suggesting a potentially large effect as bacterial grazers in those locations. This study is the first to report abundances and distributions of mixotrophic flagellates in the Southern Ocean. The presence of MNF in every ice and water sample examined suggests that mixotrophy is an important alternative dietary strategy in this region.

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Article

Characterization of protistan assemblages in the Ross Sea, Antarctica, by denaturing gradient gel electrophoresis

2004-04 , Gast, Rebecca J. , Dennett, Mark R. , Caron, David A.

The diversity of protistan assemblages has traditionally been studied using microscopy and morphological characterization, but these methods are often inadequate for ecological studies of these communities because most small protists inherently lack adequate taxonomic characters to facilitate their identification at the species level and many protistan species also do not preserve well. We have therefore used a culture-independent approach (denaturing gradient gel electrophoresis [DGGE]) to obtain an assessment of the genetic composition and distribution of protists within different microhabitats (seawater, meltwater or slush on sea-ice floes, and ice) of the Ross Sea, Antarctica. Samples of the same type (e.g., water) shared more of the same bands than samples of different types (e.g., ice versus water), despite being collected from different sites. These findings imply that samples from the same environment have a similar protistan species composition and that the type of microenvironment significantly influences the protistan species composition of these Antarctic assemblages. It should be noted that a large number of bands among the samples within each microhabitat were distinct, indicating the potential presence of significant genetic diversity within each microenvironment. Sequence analysis of selected DGGE bands revealed sequences that represent diatoms, dinoflagellates, ciliates, flagellates, and several unidentified eukaryotes.

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Article

Diel transcriptional oscillations of light-sensitive regulatory elements in open-ocean eukaryotic plankton communities

2021-02-09 , Coesel, Sacha N. , Durham, Bryndan P. , Groussman, Ryan D. , Hu, Sarah K. , Caron, David A. , Morales, Rhonda L. , Ribalet, François , Armbrust, E. Virginia

The 24-h cycle of light and darkness governs daily rhythms of complex behaviors across all domains of life. Intracellular photoreceptors sense specific wavelengths of light that can reset the internal circadian clock and/or elicit distinct phenotypic responses. In the surface ocean, microbial communities additionally modulate nonrhythmic changes in light quality and quantity as they are mixed to different depths. Here, we show that eukaryotic plankton in the North Pacific Subtropical Gyre transcribe genes encoding light-sensitive proteins that may serve as light-activated transcription factors, elicit light-driven electrical/chemical cascades, or initiate secondary messenger-signaling cascades. Overall, the protistan community relies on blue light-sensitive photoreceptors of the cryptochrome/photolyase family, and proteins containing the Light-Oxygen-Voltage (LOV) domain. The greatest diversification occurred within Haptophyta and photosynthetic stramenopiles where the LOV domain was combined with different DNA-binding domains and secondary signal-transduction motifs. Flagellated protists utilize green-light sensory rhodopsins and blue-light helmchromes, potentially underlying phototactic/photophobic and other behaviors toward specific wavelengths of light. Photoreceptors such as phytochromes appear to play minor roles in the North Pacific Subtropical Gyre. Transcript abundance of environmental light-sensitive protein-encoding genes that display diel patterns are found to primarily peak at dawn. The exceptions are the LOV-domain transcription factors with peaks in transcript abundances at different times and putative phototaxis photoreceptors transcribed throughout the day. Together, these data illustrate the diversity of light-sensitive proteins that may allow disparate groups of protists to respond to light and potentially synchronize patterns of growth, division, and mortality within the dynamic ocean environment.

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Development and application of a monoclonal-antibody technique for counting Aureococcus anophagefferens, an alga causing recurrent brown tides in the Mid-Atlantic United States

2003-09 , Caron, David A. , Dennett, Mark R. , Moran, Dawn M. , Schaffner, Rebecca A. , Lonsdale, Darcy J. , Gobler, Christopher J. , Nuzzi, Robert , McLean, Tim I.

A method was developed for the rapid detection and enumeration of Aureococcus anophagefferens, the cause of harmful algal blooms called "brown tides" in estuaries of the Mid-Atlantic United States. The method employs a monoclonal antibody (MAb) and a colorimetric, enzyme-linked immunosorbent assay format. The MAb obtained exhibits high reactivity with A. anophagefferens and very low cross-reactivities with a phylogenetically diverse array of other protists and bacteria. Standard curves are constructed for each 96-well microtiter plate by using known amounts of a preserved culture of A. anophagefferens. This approach allows estimation of the abundance of the alga in natural samples. The MAb method was compared to an existing method that employs polyclonal antibodies and epifluorescence microscopy and to direct microscopic counts of A. anophagefferens in samples with high abundances of the alga. The MAb method provided increased quantitative accuracy and greatly reduced sample processing time. A spatial survey of several Long Island estuaries in May 2000 using this new approach documented a range of abundances of A. anophagefferens in these bays spanning nearly 3 orders of magnitude.

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The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP) : illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing

2014-06-24 , Keeling, Patrick J. , Burki, Fabien , Wilcox, Heather M. , Allam, Bassem , Allen, Eric E. , Amaral-Zettler, Linda A. , Armbrust, E. Virginia , Archibald, John M. , Bharti, Arvind K. , Bell, Callum J. , Beszteri, Bank , Bidle, Kay D. , Cameron, Connor T. , Campbell, Lisa , Caron, David A. , Cattolico, Rose Ann , Collier, Jackie L. , Coyne, Kathryn J. , Davy, Simon K. , Deschamps, Phillipe , Dyhrman, Sonya T. , Edvardsen, Bente , Gates, Ruth D. , Gobler, Christopher J. , Greenwood, Spencer J. , Guida, Stephanie M. , Jacobi, Jennifer L. , Jakobsen, Kjetill S. , James, Erick R. , Jenkins, Bethany D. , John, Uwe , Johnson, Matthew D. , Juhl, Andrew R. , Kamp, Anja , Katz, Laura A. , Kiene, Ronald P. , Kudryavtsev, Alexander N. , Leander, Brian S. , Lin, Senjie , Lovejoy, Connie , Lynn, Denis , Marchetti, Adrian , McManus, George , Nedelcu, Aurora M. , Menden-Deuer, Susanne , Miceli, Cristina , Mock, Thomas , Montresor, Marina , Moran, Mary Ann , Murray, Shauna A. , Nadathur, Govind , Nagai, Satoshi , Ngam, Peter B. , Palenik, Brian , Pawlowski, Jan , Petroni, Giulio , Piganeau, Gwenael , Posewitz, Matthew C. , Rengefors, Karin , Romano, Giovanna , Rumpho, Mary E. , Rynearson, Tatiana A. , Schilling, Kelly B. , Schroeder, Declan C. , Simpson, Alastair G. B. , Slamovits, Claudio H. , Smith, David R. , Smith, G. Jason , Smith, Sarah R. , Sosik, Heidi M. , Stief, Peter , Theriot, Edward , Twary, Scott N. , Umale, Pooja E. , Vaulot, Daniel , Wawrik, Boris , Wheeler, Glen L. , Wilson, William H. , Xu, Yan , Zingone, Adriana , Worden, Alexandra Z.

Microbial ecology is plagued by problems of an abstract nature. Cell sizes are so small and population sizes so large that both are virtually incomprehensible. Niches are so far from our everyday experience as to make their very definition elusive. Organisms that may be abundant and critical to our survival are little understood, seldom described and/or cultured, and sometimes yet to be even seen. One way to confront these problems is to use data of an even more abstract nature: molecular sequence data. Massive environmental nucleic acid sequencing, such as metagenomics or metatranscriptomics, promises functional analysis of microbial communities as a whole, without prior knowledge of which organisms are in the environment or exactly how they are interacting. But sequence-based ecological studies nearly always use a comparative approach, and that requires relevant reference sequences, which are an extremely limited resource when it comes to microbial eukaryotes. In practice, this means sequence databases need to be populated with enormous quantities of data for which we have some certainties about the source. Most important is the taxonomic identity of the organism from which a sequence is derived and as much functional identification of the encoded proteins as possible. In an ideal world, such information would be available as a large set of complete, well-curated, and annotated genomes for all the major organisms from the environment in question. Reality substantially diverges from this ideal, but at least for bacterial molecular ecology, there is a database consisting of thousands of complete genomes from a wide range of taxa, supplemented by a phylogeny-driven approach to diversifying genomics. For eukaryotes, the number of available genomes is far, far fewer, and we have relied much more heavily on random growth of sequence databases, raising the question as to whether this is fit for purpose.

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Thesis

The role of heterotrophic microflagellates in plankton communities

1984-06 , Caron, David A.

The distribution and feeding behavior of bacterivorous micro flagellates (2-20 μm protozoa) and their ingestion by copepods were examined in an attempt to assess the importance of these protozoa as a trophic link between planktonic bacteria and zooplankton. The abundance of microflagellates relative to other picoplankton (0.2-2.0 μm) and nanoplankton (2-20 μm) populations in water samples in the North Atlantic and in Lake Ontario and on macroaggregates in the North Atlantic was determined using direct microscopical and culture estimation techniques. Seasonal, vertical and geographical changes in the density of microflagellates were generally not greater than one order of magnitude. Microscopical counts of heterotrophic nanoplankton (presumably microflagellates) typically ranged from a few hundred to a few thousand m1-1 for a variety of planktonic environments. They constituted approximately 1/3 to 1/2 of the nanoplankton in the euphotic zone and dominated the nanoplankton in the aphotic zone. Most Probable Number (MPN) estimation of the density of bacterivorous protozoa indicated that microflagellates were, on average, an order of magnitude more abundant than bacterivorous ciliates and amoebae. MPN and direct microscopical counts of microflagellates differed by as much as 104. This discrepancy was smaller in eutrophic environments (e.g. Continental Shelf and Lake Ontario) and on macroscopic detrital aggregates. All microbial populations enumerated were highly concentrated on macroscopic detrital aggregates relative to their abundance in the water surrounding the aggregates. Enrichment factors (the ratio of abundance of a population on a macroaggregate to its abundance in the surrounding water) increased along a eutrophic-to-oligotrophic gradient because of the combined effects of an increased abundance of microorganisms on macroaggregates in oligotrophic environments and a decreased abundance in the surrounding water in these same environments. Average enrichment factors for direct microscopical counts of heterotrophic nanoplankton (range = 17-114) were not as large as enrichment factors observed for MPN estimates of the number of bacterivorous microflagellates (range = 273-18400). Microflagellates numerically dominated the bacterivorous protozoa cultured from macroaggregates by one to two orders of magnitude, but ciliates and amoebae were also highly enriched on macroaggregates. Microenvironments are therefore a potentially important aspect for the ecology of planktonic microorganisms. Observations on the microbial colonization of mucus sloughed by ctenophores and discarded appendicularian houses suggest that these materials may be important sources of macroaggregates. Batch and continuous culture experiments were conducted with clonal cultures of microflagellates to test their ability to grow on various types and densities of bacteria. The doubling time of Monas sp. 1 ranged from 43 hr (when fed the cyanobacterium Synechococcus Strain WH 8101) to 6.9 hr (when fed the heterotrophic bacterium Serratia marinorubra). Cell yields (i.e. the conversion of bacterial biomass into protozoan biomass) of Monas sp. 1 fed two species of heterotrophic bacteria were greater than yields for the microflagellate fed two species chroococcoid cyanobacteria (range = 7-68%). Cell yields of two other species of microflagellates (Monas sp. 2 and Cryptobia maris) were 48% and 61%, respectively, on the bacterium Pseudomonas halodurans. Microflagellates grew in continuous culture at concentrations of bacteria which were lower than bacterial densities required for the growth of ciliates as shown by other investigations. Therefore, microflagellates appear to be well-adapted for grazing bacterioplankton. Microflagellates were also investigated for their ability to graze bacteria attached to particles. Bodo nanorensis and Rhynchomonas nasuta both showed a marked ability to graze attached bacteria and a limited ability to graze unattached cells. These results suggest that microflagellates may also be important consumers of bacteria attached to particles in the plankton and may explain the highly elevated densities of microflagellates on macroaggregates. Grazing experiments performed with the copepod Acartia tonsa indicated that heterotrophic microflagellates were ingested by the copepods at rates comparable to the ingestion of phytoplankton of similar size. The presence of heterotrophic microflagellates did not depress filtration rates of the copepods, and one species (Cryptobia maris) appeared to be selectively grazed. Survival of A. tonsa on a diet of heterotrophic microflagellates was similar to survival on a diet of phytoplankton and was significantly longer than survival of starved Controls or copepods fed only bacteria. Due to their ability to grow at in-situ densities of planktonic bacteria, their relatively high cell yields, and their acceptability as food for zooplankton, it is concluded that bacterivorous microflagellates may constitute an important trophic link between bacteria and zooplankton. This link may provide a mechanism whereby organic material and energy from the detrital food chain can be returned to the classical phytoplankton-copepod-fish food chain.

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