Ph.D. 1998, European Institute of Marine Sciences,
University of Western Brittany, Brest, France
Pathobiology and Immunobiology of Marine Shellfish
My research interests are centered on interactions between marine mollusks and waterborne microorganisms in general and in the framework of host-pathogen interactions in particular, including the mechanisms of resistance to pathogens and diseases (i.e. immunity), and the effect of environmental factors on these interactions. My current projects encompass host/microbe interactions at different scales, and my approach to addressing these issues involves field studies and laboratory experiments. Because of the specific diagnostic and service responsibilities of my position at Stony Brook University, my research also includes a strong applied component aimed at enhancing knowledge and development of mitigation strategies for diseases affecting local shellfish species. These activities use a diverse range of experimental and technical approaches ranging from ecological physiology and traditional pathobiology and immunology to modern “omics” tools and methods.
I am fundamentally interested in the early interactions between marine bivalves and waterborne microorganisms at mucus-rich water-tissue interfaces. An efficient processing of waterborne microbes by “slimy” water-processing organs (e.g. gills, mantle, palps) is essential for bivalves to maintain their health given the extraordinarily large number of microbes they encounter through their suspension-feeding (for example, oysters can filter over 10 L/h/g dry tissue equating over 25,000 microbes/second considering a 1 g oyster and a modest 10^4 microbes/ ml seawater, microbial concentrations are often orders of magnitude higher). In this framework, we have been looking into factors that regulate the colonization and invasion of host tissues (in particular mucosal factors), where we showed that some adapted parasites hijack host immune factors to facilitate infection.
My interests in bivalve’s water-processing organs led to the development of another axis of research that specifically focuses on the interactions between suspension-feeding bivalves and suspended particles in the framework of predator-prey interactions. This research targets long-standing questions regarding the mechanisms used by suspension-feeding bivalves to sort food particles and selectively ingest nutritive microalgae. Here we demonstrated that particle selection and sorting can be mediated by immune-related molecules, namely pattern recognition molecules (e.g. lectins), associated with mucus covering pallial organs. Using quantitative proteomic methods, we are evaluating if and how mucus composition changes in response to intrinsic and extrinsic factors and how these changes provide feedback for food uptake and microbial homeostasis at the water-tissue interface.
I have been also developing applied research on diseases affecting shellfish resources in New York State. An illustration of these activities is our investigations of Quahog Parasite Unknown (QPX), a fatal protistan parasite affecting the hard clam, Mercenaria mercenaria. This multi-faceted research and monitoring program generated information regarding the molecular, physiological and ecological characteristics of this host-parasite association. These investigations resulted in the development of significant molecular resources for the species (RNASeq studies, development of an oligoarray platform, new detection techniques, etc.). We were also able to demonstrate the genetic basis for disease resistance in clams and for the virulence of the parasite, and unravel environmental factors affecting disease progress. We are now developing molecular markers (SNPs) for disease resistance and are working on establishing field-applicable methods for disease mitigation.
The impact of environmental factors (including global climate) on immunity and infectious diseases has also been the focus of additional studies in other shellfish species such the American lobster and the eastern oyster. Research is also underway to evaluate the physiological mechanisms underlying the sensitivity or resistance of different species (or strains within the same species) to the continuously changing environment.
Funding agencies sponsoring current activities include the National Science Foundation, the National Atmospheric and Oceanographic Administration, the United State Department of Agriculture, the New York State Department of Environmental Conservation, and the Gordon and Betty Moore Foundation. For more information about these projects and other activities, please visit: http://you.stonybrook.edu/madl
Publications (since 2009, full list available at: http://you.stonybrook.edu/madl/publications/)
Pales Espinosa E, Cerrato R, Wikfors G, Allam B. (2016). Modeling food choice in the two suspension-feeding bivalves, Crassostrea virginica and Mytilus edulis. Marine Biology, 163(2): 1-13.
Wang K, Del Castillo C, Corre E, Pales Espinosa E, Allam B. (2016). Clam focal and systemic immune responses to QPX by RNA-Seq technology. BMC Genomics. In press.
Liu Q, Collier JL, Allam B. (2016). Seasonality of QPX disease in the Raritan Bay (NY) wild hard clam (Mercenaria mercenaria) population. Aquaculture Research. DOI: 10.1111/are.12969. In Press.
Wang K, Pales Espinosa E, Tanguy A, Allam B. (2016). Alterations of the immune transcriptome in resistant and susceptible hard clams (Mercenaria mercenaria) in response to Quahog Parasite Unknown (QPX) and temperature. Fish and Shellfish Immunology 49: 163-176.
Pales Espinosa E, Koller A, Allam B. (2016). Proteomic characterization of mucosal secretions in the eastern oyster, Crassostrea virginica. Journal of Proteomics 132: 63-76.
Allam B, Raftos D. (2015). Immune responses to infectious diseases in bivalves. Journal of Invertebrate Pathology 131: 121-136.
Dahl S, Allam B. (2015). Clam transplant as a mitigation strategy for QPX disease in Mercenaria mercenaria. Aquaculture Research. In Press. doi:10.1111/are.12793
Mars M, McElroy A, Pales Espinosa E, Allam B. (2015). Antimicrobial activity in the cuticle of the American lobster, Homarus americanus. Fish and Shellfish Immunology 44: 542-546.
Allam B, Pales Espinosa E. (2015). Mucosal immunity in mollusks. Book chapter In: Mucosal Health in Aquaculture. Benjamin Beck and Eric Peatman (Eds). Academic Press. pp. 325-370. ISBN: 978-0-12-417186-2.
Rubin E, Pales Espinosa E, Koller A, Allam B (2015). Characterization of the secretome of the clam parasite QPX. International Journal for Parasitology 45: 187-196.
Allam B, Tanguy A, Jeffroy F, Le Bris C, Pales Espinosa E, Paillard C. (2014). Transcriptional changes in Manila clam (Ruditapes philippinarum) in response to brown ring disease. Fish and Shellfish Immunology 41(1): 2-11.
Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, et al. (2014). The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biology, 12(6), e1001889.
Pales Espinosa E., Corre E, Allam B. (2014). Pallial mucus of Crassostrea virginica regulates the expression of putative virulence genes of its pathogen Perkinsus marinus. International Journal for Parasitology 44: 305-317.
Rubin E, Tanguy A, Perrigault M, Pales Espinosa E, Allam B. (2014). Characterization of the transcriptome and temperature-induced differential gene expression of in quahog parasite unknown QPX, the thraustochytrid parasite of hard clams. BMC Genomics 15: 245.
Pales Espinosa E, Boutet I, Le Panze S, Allam B., Tanguy A. (2013). Endobacteria in Loripes lacteus: Characterization, localization and some aspect of host-symbiont regulation. Journal of Experimental Marine Biology and Ecology 448: 327-336.
Levinton J, Doall M, Allam B. (2013). The two-year eastern oyster mortality syndrome in impacted waters. Journal of Shellfish Research 32(2): 417-427.
Rosa M, Ward JE, Shumway SS, Wikfors GH, Pales Espinosa E, Allam B. (2013). Effects of Particle Surface Properties on Feeding Selectivity in the Eastern oyster Crassostrea virginica and the Blue mussel Mytilus edulis. Journal of Experimental Marine Biology and Ecology 446: 320-327.
Pales Espinosa E., Winnicki S, Allam B. (2013). Early host-pathogen interactions in marine bivalves: Pallial mucus of Crassostrea virginica modulates the growth and virulence of its pathogen Perkinsus marinus. Diseases of Aquatic Organisms 104: 237-247.
Pales Espinosa E., Allam B. (2013). Food quality and season affect the expression of the mucosal lectin MeML and food sorting abilities in the blue mussel Mytilus edulis. Marine Biology 160(6): 144
Allam B, Carden WE, Ward JE, Ralph G, Winnicki S, Pales Espinosa E. (2013). Early host-pathogen interactions in marine bivalves: Evidence that the alveolate parasite Perkinsus marinus infects through the oyster mantle during rejection of pseudofeces. Journal of Invertebrate Pathology 113: 26-34.
Allam B , Carden WE, Ward JE, Ralph G, Winnicki S, Pales Espinosa E. (2013). Early host-pathogen interactions in marine bivalves: Evidence that the alveolate parasite Perkinsus marinus infects through the oyster mantle during rejection of pseudofeces. Journal of Invertebrate Pathology 113: 26-34.
Pales Espinosa E., Allam B.(2013). Food quality and season affect the expression of the mucosal lectin MeML and food sorting abilities in the blue mussel Mytilus edulis. Marine Biology . In Press. DOI: 10.1007/s00227-013-2196-6.
Perrigault M., Dahl S.F., Pales-Espinosa E., Allam B. (2012). Effects of salinity on hard clam (Mercenaria mercenaria) defense parameters and QPX disease dynamics. Journal of Invertebrate Pathology 110(1): 73-82.
Perrigault M, Allam B. (2012). Differential immune response in the hard clam (Mercenaria mercenaria) against bacteria and the protistan QPX (Quahog Parasite Unknown). Fish and Shellfish Immunology 32(6): 1124-1134.
Homerding M, McElroy A, Taylor G, Dove A, Allam B. (2012). Investigation of epizootic shell disease in American lobsters ( Homarus americanus ) from Long Island Sound: II. Immune parameters in lobsters and relationships to the disease. Journal of Shellfish Research31(2):495-504.
Bell SL, Allam B. , McElroy A, Dove A, Taylor GT. (2012). Investigation of epizootic shell disease in American lobsters (Homarus americanus) from Long Island Sound: I. Characterization of associated microbial communities. Journal of Shellfish Research 31(2):473-484.
Sokolowski M, Allam B, Dunton K, Clark M, Kurtz E, Fast M. (2012). Spatio-temporal differences in immunophysiology of Atlantic sturgeon, Acipenser oxyrinchus oxyrinchus (Mitchill), and the relationship to parasitic copepod, Dichelesthium oblongum, (Abilgaard) infection. Journal of Fish Diseases 35(9): 649-660.
Levinton J, Doall M, Ralston D, Starke A, Allam B. (2011). Climate change, precipitation and the loss of an estuarine refuge. PLoS One 6(4): e18849.
Dahl S, Perrigault M, Liu Q, Collier JL, Barnes DA, Allam B. (2011). Effects of temperature on hard clam ( Mercenaria mercenaria ) immunity and QPX (Quahog parasite unknown) disease development: I. Dynamics of QPX disease. Journal of Invertebrate Pathology106: 314-321.
Perrigault M., Dahl S.F., Pales Espinosa E., Gambino L., Allam B. (2011). Effects of temperature on hard clam ( Mercenaria mercenaria) immunity and QPX (Quahog parasite unknown) disease development: II. Defense parameters. Journal of Invertebrate Pathology 106: 322-332.
Jing X, Pales Espinosa E, Perrigault M, Allam B. (2011). Identification, molecular characterization and expression analysis of a mucosal C-type lectin in the eastern oyster, Crassostrea virginica . Fish and Shellfish Immunology 30: 851-858.
Pales Espinosa E, Perrigault M, Ward JE, Shumway S, Allam B. (2010). Lectin binding patterns of microalgae: role in particle selection in suspension feeding bivalves. Biological Bulletin 218: 75-86.
Dahl S, Thiel J., Allam B. (2010). QPX disease progress in cultured and wild type hard clams in New York waters. Journal of Shellfish Research 29(1): 83-90.
Perrigault M, Buggé DM., Allam B. (2010). Effect of environmental factors on survival and growth of quahog parasite unknown (QPX) in vitro. Journal of Invertebrate Pathology 104: 83-89.
Pales Espinosa E, Perrigault M, Allam B. (2010). Identification and molecular characterization of a mucosal lectin (MeML) from Mytilus edulis and its potential role in particle capture. Comparative Biochemistry and Physiology 156: 495-501.
Pales Espinosa E, Hassan D, Ward JE, Shumway SE, Allam B. (2010). The blue mussel Mytilus edulis uses recognition molecules to select food particles. Biological Bulletin 219: 50-60.
Perrigault M, Buggé DM, Hao CC, Allam B. (2009). Modulatory effects of hard clam (Mercenaria mercenaria ) tissue extracts on the in vitro growth of its pathogen QPX. Journal of Invertebrate Pathology 100: 1-8.
Bettencourt R, Dando P, Collins P, Costa V, Allam B, Serrão Santos R. (2009). Innate immunity in the deep sea hydrothermal vent mussel Bathymodiolus azoricus . Comparative Biochemistry and Physiology Part A 152: 278-289.
Ford SE, Allam B, Xu Z. (2009). Using PCR and bivalve “particle collectors” to investigate the environmental distribution ofHaplosporidium nelsoni, the agent of MSX disease in eastern oysters. Diseases of Aquatic Organisms 83: 159-168.
Liu Q, Allam B. , Collier JL. (2009). A quantitative real-time PCR assay for QPX (Thraustochytridae), a parasite of the hard clam (Mercenaria mercenaria ). Applied and Environmental Microbiology 75: 4913-4918.
Perrigault M, Allam B. (2009). Cytotoxicity of Quahog Parasite Unknown (QPX) toward hard clam ( Mercenaria mercenaria ) haemocytes and interactions between different pathogen isolates and host strains. Parasitology 136: 1281-1289.
Pales Espinosa, E., Perrigault, M., Ward, J.E., Shumway, S.E., Allam, B. (2009). Lectins associated with the feeding organs of the oysterCrassostrea virginica can mediate particle selection. Biological Bulletin 217: 130-141.
Perrigault M, Tanguy A, Allam B. (2009). Indentification and quantification of differentially expressed genes in the hard clam,Mercenaria mercenaria , in response to quahog parasite unknown (QPX). BMC Genomics 10: 377. doi:10.1186/1471-2164-10-377
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