Johnson Matthew D.

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Mesodinium rubrum exhibits genus-level but not species-level cryptophyte prey selection

(Inter-Research, 2017-02-09) Peltomaa, Elina ; Johnson, Matthew D.

The marine ciliate Mesodinium rubrum is known to form large non-toxic red water blooms in estuarine and coastal upwelling regions worldwide. This ciliate relies predominantly upon photosynthesis by using plastids and other organelles it acquires from cryptophyte prey. Although M. rubrum is capable of ingesting different species of cryptophytes, mainly Teleaulax amphioxeia plastids have been detected from wild M. rubrum populations. These observations suggest that either M. rubrum is a selective feeder, or T. amphioxeia are taken up because of higher availability. To test these hypotheses, we determined whether the ciliate showed different grazing rates, growth responses, or plastid retention dynamics when offered Storeatula major, T. amphioxeia, T. acuta, or a mix. When M. rubrum was offered the cryptophyte S. major as prey, no evidence was found for ingestion. In contrast, M. rubrum grazed both Teleaulax spp. equally, was able to easily switch plastid type between them, and the ratio of each in the ciliate reflected the abundance of free-living prey in the culture. M. rubrum grew equally well when acclimated to each plastid type or when having mixed plastids. However, when offered single prey, T. amphioxeia could sustain higher M. rubrum growth rates (μ) over longer periods. Compared to other M. rubrum strains, this culture had higher grazing rates, greater ingestion requirements for reaching μmax, and appeared to rely more on plastid sequestration than de novo division of cryptophyte organelles. Our results suggest that while M. rubrum may prefer Teleaulax-like cryptophytes, they do not select among the species used here.
Acquired phototrophy in aquatic protists

(Inter-Research, 2009-11-24) Stoecker, Diane K. ; Johnson, Matthew D. ; de Vargas, Colomban ; Not, Fabrice

Acquisition of phototrophy is widely distributed in the eukaryotic tree of life and can involve algal endosymbiosis or plastid retention from green or red origins. Species with acquired phototrophy are important components of diversity in aquatic ecosystems, but there are major differences in host and algal taxa involved and in niches of protists with acquired phototrophy in marine and freshwater ecosystems. Organisms that carry out acquired phototrophy are usually mixotrophs, but the degree to which they depend on phototrophy is variable. Evidence suggests that ‘excess carbon’ provided by acquired phototrophy has been important in supporting major evolutionary innovations that are crucial to the current ecological roles of these protists in aquatic ecosystems. Acquired phototrophy occurs primarily among radiolaria, foraminifera, ciliates and dinoflagellates, but is most ecologically important among the first three. Acquired phototrophy in foraminifera and radiolaria is crucial to their contributions to carbonate, silicate, strontium, and carbon flux in subtropical and tropical oceans. Planktonic ciliates with algal kleptoplastids are important in marine and fresh waters, whereas ciliates with green algal endosymbionts are mostly important in freshwaters. The phototrophic ciliate Myrionecta rubra can be a major primary producer in coastal ecosystems. Our knowledge of how acquired phototrophy influences trophic dynamics and biogeochemical cycles is rudimentary; we need to go beyond traditional concepts of ‘plant’ and ‘animal’ functions to progress in our understanding of aquatic microbial ecology. This is a rich area for exploration using a combination of classical and molecular techniques, laboratory and field research, and physiological and ecosystem modeling.
Seasonal dynamics of Mesodinium rubrum in Chesapeake Bay

( 2013-03) Johnson, Matthew D. ; Stoecker, Diane K. ; Marshall, Harold G.

The photosynthetic ciliate Mesodinium rubrum is a common member of coastal phytoplankton communities that is well adapted to low-light, turbid ecosystems. It supports the growth of or competes with harmful dinoflagellate species for cryptophyte prey, as well as being a trophic link to copepods and larval fish. We have compiled data from various sources (n = 1063), on the abundance and distribution of M. rubrum in Chesapeake Bay and its tributaries. Because M. rubrum relies on obtaining organelles from cryptophyte algae to maintain rapid growth, we also enumerated cryptophyte algae in the portion of these samples that we collected (n = 386). M. rubrum occurred in oligohaline to polyhaline regions of Chesapeake Bay and throughout the year. Blooms (>100 cells ml-1) of M. rubrum primarily occurred during spring, followed by autumn. When compared across all seasons, M. rubrum abundance was positively correlated to temperature and cryptophytes, and negatively correlated with salinity. However, more focused analyses revealed that M. rubrum abundance during spring was associated with surface layer warming and decreased salinity, while early autumn assemblages were associated with surface cooling. These results imply there are distinct seasonal niches for M. rubrum blooms. Blooms of M. rubrum were more common in tributaries than in the main stem Bay and tended to be restricted to salinities under 10 PSU. Despite the rarity of “red water” events, M. rubrum is a ubiquitous mixotroph in Chesapeake Bay and at times likely exerts a strong influence on cryptophyte algal abundance and hence planktonic food web structure.
Marine cryptophytes are great sources of EPA and DHA

(MDPI AG, 2017-12-26) Peltomaa, Elina ; Johnson, Matthew D. ; Taipale, Sami J.

Microalgae have the ability to synthetize many compounds, some of which have been recognized as a source of functional ingredients for nutraceuticals with positive health effects. One well-known example is the long-chain polyunsaturated fatty acids (PUFAs), which are essential for human nutrition. Eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) are the two most important long-chain omega-3 (ω-3) PUFAs involved in human physiology, and both industries are almost exclusively based on microalgae. In addition, algae produce phytosterols that reduce serum cholesterol. Here we determined the growth rates, biomass yields, PUFA and sterol content, and daily gain of eight strains of marine cryptophytes. The maximal growth rates of the cryptophytes varied between 0.34–0.70 divisions day−1, which is relatively good in relation to previously screened algal taxa. The studied cryptophytes were extremely rich in ω-3 PUFAs, especially in EPA and DHA (range 5.8–12.5 and 0.8–6.1 µg mg dry weight−1, respectively), but their sterol concentrations were low. Among the studied strains, Storeatula major was superior in PUFA production, and it also produces all PUFAs, i.e., α-linolenic acid (ALA), stearidonic acid (SDA), EPA, and DHA, which is rare in phytoplankton in general. We conclude that marine cryptophytes are a good alternative for the ecologically sustainable and profitable production of health-promoting lipids.
The acquisition of phototrophy : adaptive strategies of hosting endosymbionts and organelles

( 2010-04) Johnson, Matthew D.

Many non-photosynthetic species of protists and metazoans are capable of hosting viable algal endosymbionts or their organelles through adaptations of phagocytic pathways. A form of mixotrophy, acquired phototrophy (AcPh) encompasses a sweet of endosymbiotic and organelle retention interactions, that range from facultative to obligate. AcPh is a common phenomenon in aquatic ecosystems, with endosymbiotic associations generally more prevalent in nutrient poor environments, and organelle retention typically associated with more productive ones. All AcPhs benefit from enhanced growth due to access to photosynthetic products, however the degree of metabolic integration and dependency in the host varies widely. AcPhs are mixotrophic, using both heterotrophic and phototrophic carbon sources. AcPh is found in at least four of the major eukaryotic supergroups, and is the driving force in the evolution of secondary and tertiary plastid acquisitions. Mutualistic resource partitioning characterizes most algal endosymbiotic interactions, while organelle retention is a form of predation, characterized by nutrient flow (i.e. growth) in one direction. AcPh involves adaptations to recognize specific prey or endosymbionts and to house organelles or endosymbionts within the endomembrane system but free from digestion. In many cases, hosts depend upon AcPh for the production of essential nutrients, many of which remain obscure. The practice of AcPh has led to multiple independent secondary and tertiary plastid acquisition events among several eukaryote lineages, giving rise to the diverse array of algae found in modern aquatic ecosystems. This review highlights those AcPhs that are model research organisms for both metazoans and protists. Much of the basic biology of AcPhs remains enigmatic, particularly 1) which essential nutrients or factors make certain forms of AcPh obligatory, 2) how hosts regulate and manipulate endosymbionts or sequestered organelles, and 3) what genomic imprint, if any, AcPh leaves on non-photosynthetic host species.
A bacterial quorum-sensing precursor induces mortality in the marine coccolithophore, Emiliania huxleyi

(Frontiers Media, 2016-02-03) Harvey, Elizabeth L. ; Deering, Robert W. ; Rowley, David C. ; El Gamal, Abrahim ; Schorn, Michelle A. ; Moore, Bradley S. ; Johnson, Matthew D. ; Mincer, Tracy J. ; Whalen, Kristen E.

Interactions between phytoplankton and bacteria play a central role in mediating biogeochemical cycling and food web structure in the ocean. However, deciphering the chemical drivers of these interspecies interactions remains challenging. Here, we report the isolation of 2-heptyl-4-quinolone (HHQ), released by Pseudoalteromonas piscicida, a marine gamma-proteobacteria previously reported to induce phytoplankton mortality through a hitherto unknown algicidal mechanism. HHQ functions as both an antibiotic and a bacterial signaling molecule in cell–cell communication in clinical infection models. Co-culture of the bloom-forming coccolithophore, Emiliania huxleyi with both live P. piscicida and cell-free filtrates caused a significant decrease in algal growth. Investigations of the P. piscicida exometabolome revealed HHQ, at nanomolar concentrations, induced mortality in three strains of E. huxleyi. Mortality of E. huxleyi in response to HHQ occurred slowly, implying static growth rather than a singular loss event (e.g., rapid cell lysis). In contrast, the marine chlorophyte, Dunaliella tertiolecta and diatom, Phaeodactylum tricornutum were unaffected by HHQ exposures. These results suggest that HHQ mediates the type of inter-domain interactions that cause shifts in phytoplankton population dynamics. These chemically mediated interactions, and other like it, ultimately influence large-scale oceanographic processes.
Transparent exopolymer particle (TEP) measurements from the MesoHux mesocosm experiment held in May 2017

(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2021-05-19) Johnson, Matthew D. ; Bidle, Kay D. ; Harvey, Elizabeth

Transparent exopolymer particle (TEP) measurements from the MesoHux mesocosm experiment held in May 2017. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/748500
The possession of coccoliths fails to deter microzooplankton grazers

(Frontiers Media, 2020-12-02) Mayers, Kyle M. J. ; Poulton, Alex J. ; Bidle, Kay D. ; Thamatrakoln, Kimberlee ; Schieler, Brittany ; Giering, Sarah L. C. ; Wells, Seona R. ; Tarran, Glen A. ; Mayor, Daniel J. ; Johnson, Matthew D. ; Riebesell, Ulf ; Larsen, Aud ; Vardi, Assaf ; Harvey, Elizabeth L.

Phytoplankton play a central role in the regulation of global carbon and nutrient cycles, forming the basis of the marine food webs. A group of biogeochemically important phytoplankton, the coccolithophores, produce calcium carbonate scales that have been hypothesized to deter or reduce grazing by microzooplankton. Here, a meta-analysis of mesocosm-based experiments demonstrates that calcification of the cosmopolitan coccolithophore, Emiliania huxleyi, fails to deter microzooplankton grazing. The median grazing to growth ratio for E. huxleyi (0.56 ± 0.40) was not significantly different among non-calcified nano- or picoeukaryotes (0.71 ± 0.31 and 0.55 ± 0.34, respectively). Additionally, the environmental concentration of E. huxleyi did not drive preferential grazing of non-calcified groups. These results strongly suggest that the possession of coccoliths does not provide E. huxleyi effective protection from microzooplankton grazing. Such indiscriminate consumption has implications for the dissolution and fate of CaCO3 in the ocean, and the evolution of coccoliths.
Insights into transcriptional changes that accompany organelle sequestration from the stolen nucleus of Mesodinium rubrum

(BioMed Central, 2015-10-16) Lasek-Nesselquist, Erica ; Wisecaver, Jennifer H. ; Hackett, Jeremiah D. ; Johnson, Matthew D.

Organelle retention is a form of mixotrophy that allows organisms to reap metabolic benefits similar to those of photoautotrophs through capture of algal prey and sequestration of their plastids. Mesodinium rubrum is an abundant and broadly distributed photosynthetic marine ciliate that steals organelles from cryptophyte algae, such as Geminigera cryophila. M. rubrum is unique from most other acquired phototrophs because it also steals a functional nucleus that facilitates genetic control of sequestered plastids and other organelles. We analyzed changes in G. cryophila nuclear gene expression and transcript abundance after its incorporation into the cellular architecture of M. rubrum as an initial step towards understanding this complex system. We compared Illumina-generated transcriptomes of the cryptophyte Geminigera cryophila as a free-living cell and as a sequestered nucleus in M. rubrum to identify changes in protein abundance and gene expression. After KEGG annotation, proteins were clustered by functional categories, which were evaluated for over- or under-representation in the sequestered nucleus. Similarly, coding sequences were grouped by KEGG categories/pathways, which were then evaluated for over- or under-expression via read count strategies. At the time of sampling, the global transcriptome of M. rubrum was dominated (~58–62 %) by transcription from its stolen nucleus. A comparison of transcriptomes from free-living G. cryophila cells to those of the sequestered nucleus revealed a decrease in gene expression and transcript abundance for most functional protein categories within the ciliate. However, genes coding for proteins involved in photosynthesis, oxidative stress reduction, and several other metabolic pathways revealed striking exceptions to this general decline. Major changes in G. cryophila transcript expression after sequestration by M. rubrum and the ciliate’s success as a photoautotroph imply some level of control or gene regulation by the ciliate and at the very least reflect a degree of coordination between host and foreign organelles. Intriguingly, cryptophyte genes involved in protein transport are significantly under-expressed in M. rubrum, implicating a role for the ciliate’s endomembrane system in targeting cryptophyte proteins to plastid complexes. Collectively, this initial portrait of an acquired transcriptome within a dynamic and ecologically successful ciliate highlights the remarkable cellular and metabolic chimerism of this system.
Data from an experiment that measured the occurrence of feeding among 8 Prorocentrum minimum strains on fluorescently labeled bacteria or the cryptophyte Teleaulax amphioxeia

(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2019-03-15) Johnson, Matthew D.

This dataset contains data from an experiment that measured the occurrence of feeding among 8 Prorocentrum minimum strains on fluorescently labeled bacteria or the cryptophyte Teleaulax amphioxeia. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/750823
Data from an experiment that measured the occurrence of feeding among 4 Prorocentrum minimum strains on the cryptophyte Teleaulax amphoxeia

(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2019-03-15) Johnson, Matthew D.

This dataset contains data from an experiment that measured the occurrence of feeding among 4 Prorocentrum minimum strains on the cryptophyte Teleaulax amphoxeia. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/750795
Consequences of strain variability and calcification in Emiliania huxleyi on microzooplankton grazing

( 2015-08-04) Harvey, Elizabeth L. ; Bidle, Kay D. ; Johnson, Matthew D.

Microzooplankton are the main consumers of marine phytoplankton. Intrinsic traits of phytoplankton can reduce grazing mortality, directly influencing phytoplankton population dynamics, food web ecology, and biogeochemical cycling. We examined the impact of calcification in mediating the functional grazing response of three heterotrophic dinoflagellates, on the coccolithophore, Emilania huxleyi. A variety of parameters, including predator grazing and growth rates, were examined over a 24-48 h period, at 1-5 prey concentrations for five isolates of E. huxleyi that fell along a gradient of calcification states. Significant differences in ingestion and clearance rate were strain-specific, and no apparent trends were observed in relation to calcification. However, predators had, on average, a had a 60% slower growth rate on calcified strains relative to naked strains; furthermore, gross growth efficiency was reduced when ingesting calcified strains. A growth rate model demonstrated a positive feedback from grazing interactions whereby decreased predator growth rate on calcified strains resulted in the accumulation of E. huxleyi. This study highlights the complexity involved in understanding the role of prey phenotype on grazing rates, and emphasizes the importance in considering morphological traits when deciphering predator-prey interactions in the plankton.
The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP) : illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing

(Public Library of Science, 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.
Evidence for strain-specific exometabolomic responses of the coccolithophore Emiliania huxleyi to grazing by the dinoflagellate oxyrrhis marina

(Frontiers Media, 2016-01-28) Poulson-Ellestad, Kelsey L. ; Harvey, Elizabeth L. ; Johnson, Matthew D. ; Mincer, Tracy J.

The coccolithophore Emiliania huxleyi forms massive blooms and plays a critical role in global elemental cycles, sequestering significant amounts of atmospheric carbon dioxide on geological time scales via production of calcium carbonate coccoliths and emitting dimethyl sulfoniopropionate (DMSP), which has the potential for increasing atmosph-eric albedo. Because grazing in pelagic systems is a major top-down force structuring microbial communities, the influence of grazers on E. huxleyi populations has been of interest to researchers. Roles of DMSP (and related metabolites) in interactions between E. huxleyi and protist grazers have been investigated, however, little is known about the release of other metabolites that may influence, or be influenced by, such grazing interactions. We used high-resolution mass spectrometry in an untargeted approach to survey the suite of low molecular weight compounds released by four different E. huxleyi strains in response to grazing by the dinoflagellate Oxyrrhis marina. Overall, a strikingly small number of metabolites were detected from E. huxleyi and O. marina cells, but these were distinctly informative to construct metabolic footprints. At most, E. huxleyi strains shared 25% of released metabolites. Furthermore, there appeared to be no unified metabolic response in E. huxleyi strains to grazing; rather, these responses were strain specific. Concentrations of several metabolites also positively correlated with grazer activities, including grazing, ingestion, and growth rates; however, no single metabolite responded uniformly across all strains of E. huxleyi tested. Regardless, grazing clearly transformed the constituents of dissolved organic matter produced by these marine microbes. This study addresses several technical challenges, and presents a platform to further study the influence of chemical cues in aquatic systems and demonstrates the impact of strain diversity and grazing on the complexity of dissolved organic matter in marine systems.
High grazing rates on cryptophyte algae in Chesapeake Bay

(Frontiers Media, 2018-07-25) Johnson, Matthew D. ; Beaudoin, David J. ; Frada, Miguel J. ; Brownlee, Emily F. ; Stoecker, Diane K.

Cryptophyte algae are globally distributed photosynthetic flagellates found in freshwater, estuarine, and neritic ecosystems. While cryptophytes can be highly abundant and are consumed by a wide variety of protistan predators, few studies have sought to quantify in situ grazing rates on their populations. Here we show that autumnal grazing rates on in situ communities of cryptophyte algae in Chesapeake Bay are high throughout the system, while growth rates, particularly in the lower bay, were low. Analysis of the genetic diversity of cryptophyte populations within dilution experiments suggests that microzooplankton may be selectively grazing the fastest-growing members of the population, which were generally Teleaulax spp. We also demonstrate that potential grazing rates of ciliates and dinoflagellates on fluorescently labeled (FL) Rhodomonas salina, Storeatula major, and Teleaulax amphioxeia can be high (up to 149 prey predator−1 d−1), and that a Gyrodinium sp. and Mesodinium rubrum could be selective grazers. Potential grazing was highest for heterotrophic dinoflagellates, but due to its abundance, M. rubrum also had a high overall impact. This study reveals that cryptophyte algae in Chesapeake Bay can experience extremely high grazing pressure from phagotrophic protists, and that this grazing likely shapes their community diversity.
Acquired phototrophy stabilizes coexistence and shapes intrinsic dynamics of an intraguild predator and its prey

( 2015-12-10) Moeller, Holly ; Peltomaa, Elina ; Johnson, Matthew D. ; Neubert, Michael G.

In marine ecosystems, acquired phototrophs|organisms that obtain their photo- synthetic ability by hosting endosymbionts or stealing plastids from their prey|are omnipresent. Such taxa function as intraguild predators yet depend on their prey to periodically obtain chloroplasts. We present new theory for the effects of acquired phototrophy on community dynamics by analyzing a mathematical model of this predator-prey interaction and experimentally verifying its predictions with a lab- oratory model system. We show that acquired phototrophy stabilizes coexistence, but that the nature of this coexistence exhibits a `paradox of enrichment:' as light increases, the coexistence between the acquired phototroph and its prey transitions from a stable equilibrium to boom-bust cycles whose amplitude increases with light availability. In contrast, heterotrophs and mixotrophic acquired phototrophs (that obtain <30% of their carbon from photosynthesis) do not exhibit such cycles. This prediction matches eld observations, in which only strict (>95% of carbon from photosynthesis) acquired phototrophs form blooms.
Light-dependent grazing can drive formation and deepening of deep chlorophyll maxima

(Nature Research, 2019-04-24) Moeller, Holly V. ; Laufkötter, Charlotte ; Sweeney, Edward M. ; Johnson, Matthew D.

Deep Chlorophyll Maxima (DCMs) are subsurface peaks in chlorophyll-a concentration that may coincide with peaks in phytoplankton abundance and primary productivity. Work on the mechanisms underlying DCM formation has historically focused on phytoplankton physiology (e.g., photoacclimation) and behavior (e.g., taxis). While these mechanisms can drive DCM formation, they do not account for top-down controls such as predation by grazers. Here, we propose a new mechanism for DCM formation: Light-dependent grazing by microzooplankton reduces phytoplankton biomass near the surface but allows accumulation at depth. Using mathematical models informed by grazing studies, we demonstrate that light-dependent grazing is sufficient to drive DCM formation. Further, when acting in concert with other mechanisms, light-dependent grazing deepens the DCM, improving the fit of a global model with observational data. Our findings thus reveal another mechanism by which microzooplankton may regulate primary production, and impact our understanding of biogeochemical cycling at and above the DCM.
The genetic diversity of Mesodinium and associated cryptophytes

(Frontiers Media, 2016-12-20) Johnson, Matthew D. ; Beaudoin, David J. ; Laza-Martinez, Aitor ; Dyhrman, Sonya T. ; Fensin, Elizabeth ; Lin, Senjie ; Merculief, Aaron ; Nagai, Satoshi ; Pompeu, Mayza ; Setala, Outi ; Stoecker, Diane K.

Ciliates from the genus Mesodinium are globally distributed in marine and freshwater ecosystems and may possess either heterotrophic or mixotrophic nutritional modes. Members of the Mesodinium major/rubrum species complex photosynthesize by sequestering and maintaining organelles from cryptophyte prey, and under certain conditions form periodic or recurrent blooms (= red tides). Here, we present an analysis of the genetic diversity of Mesodinium and cryptophyte populations from 10 environmental samples (eight globally dispersed habitats including five Mesodinium blooms), using group-specific primers for Mesodinium partial 18S, ITS, and partial 28S rRNA genes as well as cryptophyte large subunit RuBisCO genes (rbcL). In addition, 22 new cryptophyte and four new M. rubrum cultures were used to extract DNA and sequence rbcL and 18S-ITS-28S genes, respectively, in order to provide a stronger phylogenetic context for our environmental sequences. Bloom samples were analyzed from coastal Brazil, Chile, two Northeastern locations in the United States, and the Pribilof Islands within the Bering Sea. Additionally, samples were also analyzed from the Baltic and Barents Seas and coastal California under non-bloom conditions. Most blooms were dominated by a single Mesodinium genotype, with coastal Brazil and Chile blooms composed of M. major and the Eastern USA blooms dominated by M. rubrum variant B. Sequences from all four blooms were dominated by Teleaulax amphioxeia-like cryptophytes. Non-bloom communities revealed more diverse assemblages of Mesodinium spp., including heterotrophic species and the mixotrophic Mesodinium chamaeleon. Similarly, cryptophyte diversity was also higher in non-bloom samples. Our results confirm that Mesodinium blooms may be caused by M. major, as well as multiple variants of M. rubrum, and further implicate T. amphioxeia as the key cryptophyte species linked to these phenomena in temperate and subtropical regions.
Intraguild predation enables coexistence of competing phytoplankton in a well-mixed water column

(Ecological Society of America, 2019-08-28) Moeller, Holly V. ; Neubert, Michael G. ; Johnson, Matthew D.

Resource competition theory predicts that when two species compete for a single, finite resource, the better competitor should exclude the other. However, in some cases, weaker competitors can persist through intraguild predation, that is, by eating their stronger competitor. Mixotrophs, species that meet their carbon demand by combining photosynthesis and phagotrophic heterotrophy, 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 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 limiting resource, light, is relatively high), or when species interactions are strong (i.e., attack rates and conversion efficiencies are high). Both our mathematical and laboratory models show that, depending upon the environment and species traits, a variety of equilibrium outcomes, ranging from competitive exclusion to coexistence, are possible.
Chlorophyll measurements from the MesoHux mesocosm experiment held in May 2017

(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2021-05-19) Johnson, Matthew D. ; Bidle, Kay D. ; Harvey, Elizabeth

Chlorophyll measurements from the MesoHux mesocosm experiment held in May 2017. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/748471

Johnson Matthew D.

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