Microheterogeneity and Coevolution: An Examination of rDNA Sequence Characteristics in <i>Neoparamoeba pemaquidensis</i> and Its Prokinetoplastid Endosymbiont

Caraguel, Charles; O’Kelly, Charles J.; Legendre, Pierre; Frasca, Salvatore; Gast, Rebecca J.; Despres, B.; Cawthorn, Richard J.; Greenwood, Spencer J.

doi:10.1111/j.1550-7408.2007.00281.x

Cited by 28 publications

(21 citation statements)

References 56 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Neoparamoeba pemaquidensis is an amphizoic, or facultatively parasitic, ameba found in the sediments of WLIS as well as on healthy lobsters from other locations (Gillevet and O'Kelly 2003;Mullen et al 2005;Caraguel et al 2007). The ameba likely required a portal of entry and a host with a compromised immune system.…”

Section: The 1999 Lobster Mortality In Western Long Island Sound (Wlis)mentioning

confidence: 98%

Complex etiologies of emerging diseases in lobsters (Homarus americanus) from Long Island Sound

Shields

2013

Can. J. Fish. Aquat. Sci.

View full text Add to dashboard Cite

Several diseases have recently emerged in lobsters (Homarus americanus) from Long Island Sound (LIS). Various stressors have been implicated as contributory factors, including increased bottom temperatures, extensive eutrophication with commensurate hypoxia, storm-induced thermal destratification, possible exposures to pesticides and metals, and fishery-induced stressors. Such stressors increase host susceptibility by weakening the host immune defenses and act to increase the transmission and severity of pathogens. The lobster mortality in western LIS in 1999 was linked to Neoparamoeba pemaquidensis, but a complex of stressors resulted in outright mortality from hypoxia or consequent immune suppression that increased susceptibility to the ameba. Similar stressors have been implicated in the etiology of epizootic shell disease and calcinosis. The role of environmental stressors has been hard to delineate, but recent declines in landings indicate that epizootic shell disease has had a negative impact on the lobster population in LIS. Calcinosis, blindness, and hepatopancreatitis are indicators of continued exposure to anthropogenic stressors, but their etiologies remain undetermined. More research is needed to understand emerging diseases, their complex etiologies, and their effects on the lobster population.Résumé : Plusieurs maladies sont récemment apparues chez les homards (Homarus americanus) du Long Island Sound (LIS). Plusieurs facteurs de stress ont été mis en cause comme facteurs contributifs, y compris l'augmentation des températures du fond de l'eau, une vaste eutrophication avec hypoxie à l'avenant, une déstratification thermique induite par les tempêtes, des expositions possibles à des pesticides et métaux et des facteurs de stress associés à la pêche. De tels facteurs de stress accroissent non seulement la susceptibilité des hôtes en affaiblissant leurs défenses immunitaires, mais également la transmission et l'activité des pathogènes. Si la mortalité des homards dans la partie occidentale du LIS en 1999 a été reliée à Neoparamoeba pemaquidensis, un complexe de facteurs de stress a entraîné une mortalité directe des suites de l'hypoxie ou de l'immunosuppression en découlant, qui se sont traduites par une susceptibilité accrue aux amibes. Des facteurs de stress semblables ont été mis en cause dans l'étiologie de l'épizootie de la carapace et de la calcinose. S'il s'est avéré difficile de cerner le rôle des facteurs de stress environnementaux, les baisses récentes des débarquements indiquent que l'épizootie de la carapace a eu un impact négatif sur la population de homards du LIS. La calcinose, la cécité, et l'hépatopancréatite sont autant d'indicateurs d'une exposition soutenue à des facteurs de stress d'origine humaine, mais leurs étiologies demeurent à définir. D'autres travaux sont nécessaires pour comprendre ces maladies émergentes, leurs étiologies complexes et leurs effets sur la population de homards. [Traduit par la Rédaction]

show abstract

Section: The 1999 Lobster Mortality In Western Long Island Sound (Wlis)mentioning

confidence: 98%

Complex etiologies of emerging diseases in lobsters (Homarus americanus) from Long Island Sound

Shields

2013

Can. J. Fish. Aquat. Sci.

View full text Add to dashboard Cite

show abstract

“…This phenomenon is commonly seen in plastids and mitochondria (15,32), bacterial endosymbionts, such as Buchnera (25,26,30), and eukaryotic intracellular pathogens, such as microsporidia (7,8,35). A strong signal for coevolution of Neoparamoeba-IRO pairs is clear from analyses of rDNA sequences (6,11), and given that Neoparamoeba is invariably found with at least one IRO residing within it, the relationship between the two is very likely obligate (6). How big is the IRO nuclear genome, and where does this enigmatic organism reside along the continuum between transient endosymbiont and organelle?…”

mentioning

confidence: 99%

“…We refer to this enigmatic endosymbiont as the "Ichthyobodo-related organism" (IRO) based on 18S ribosomal DNA (rDNA) analyses showing its close affinity to Ichthyobodo (6,(10)(11)(12). In this study we characterized genes from N. pemaquidensis and its kinetoplastid endosymbiont and carried out the first investigation of the chromosomes of both organisms using pulsed-field gel electrophoresis (PFGE) and Southern blotting.…”

mentioning

confidence: 99%

Genomic Characterization of Neoparamoeba pemaquidensis (Amoebozoa) and Its Kinetoplastid Endosymbiont

et al. 2011

Self Cite

View full text Add to dashboard Cite

We have performed a genomic characterization of a kinetoplastid protist living within the amoebozoan Neoparamoeba pemaquidensis. The genome of this "Ichthyobodo-related organism" was found to be unexpectedly large, with at least 11 chromosomes between 1.0 and 3.5 Mbp and a total genome size of at least 25 Mbp.Kinetoplastids are an important group of eukaryotic microbes named by virtue of their shared possession of a conspicuous mass of DNA-the "kinetoplast"-inside the mitochondrion (21, 31). They are remarkable for their bizarre suite of biochemical features (e.g., spliced leader [SL] trans splicing and mitochondrial RNA editing) (1,5,21) and are best known as pathogens: the so-called "tritryps" are responsible for mass mortality and morbidity in humans and other animals (1, 14, 31). The kinetoplastids also contain a variety of other parasites, such as the fish pathogen Cryptobia, as well as many free-living groups (e.g., Bodo) (31). Phylogenetic studies suggest that within kinetoplastids, parasitic lineages have evolved from free-living ones on at least four occasions (31). Despite many genomics-enabled advances for the tritryp pathogens (e.g., see references 2, 14, and 18), a comprehensive evolutionary framework for understanding the biology of these important pathogens is currently lacking.The kinetoplastid endosymbiont of Neoparamoeba pemaquidensis, an amoebozoan that causes disease in fish (e.g., Atlantic salmon) and invertebrates such as lobster (20,27), represents an apparent example of "recent" adaptation to intracellularity. We refer to this enigmatic endosymbiont as the "Ichthyobodo-related organism" (IRO) based on 18S ribosomal DNA (rDNA) analyses showing its close affinity to Ichthyobodo (6,(10)(11)(12). In this study we characterized genes from N. pemaquidensis and its kinetoplastid endosymbiont and carried out the first investigation of the chromosomes of both organisms using pulsed-field gel electrophoresis (PFGE) and Southern blotting.N. pemaquidensis strains CCAP 1560/4 and 1560/5 and Neoparamoeba branchiphila AFSM3/II were cultured as described previously (13). Using standard transmission electron microscopy (TEM) and 4Ј,6-diamidino-2-phenylindole (DAPI) staining protocols, N. pemaquidensis strain 1560/4 was mostly found to possess 1 (and only occasionally 2) oval or round IRO per cell, each 4 to 6 m in diameter. The IRO was typically very closely associated with the host cell nucleus, with their surfaces often appearing to be in direct contact (Fig. 1A and C). This is consistent with previous reports based on studies of multiple strains of Neoparamoeba (e.g., see references 10, 12, 13, and 17). Within the IRO, a single mitochondrion was found to occupy more than half of the endosymbiont cell volume, with its distinctive kinetoplast DNA (kDNA) appearing as a complex fibrillar structure in TEM micrographs (Fig. 1A and B). The close proximity of the IRO to the amoeba host nucleus was also apparent under DAPI staining (Fig. 1C). The IRO nucleus stained weakly with DAPI relative to the amoeba nucle...

show abstract

“…They are of significant economic and ecological interest because of their association with Amoebic Gill Disease (AGD) in various fishes, paramoebiasis in blue crabs and lobster, and wasting disease in green sea urchins (Caraguel et al. ; Dyková et al. ; Feehan et al.…”

mentioning

confidence: 99%

Diversity and Evolution of Paramoeba spp. and their Kinetoplastid Endosymbionts

Sibbald

Cenci

Colp

et al. 2017

J Eukaryotic Microbiology

Self Cite

View full text Add to dashboard Cite

Members of the genus Paramoeba (including Neoparamoeba) (Amoebozoa) are single-celled eukaryotes of economic and ecological importance because of their association with disease in a variety of marine animals including fish, sea urchins, and lobster. Interestingly, they harbor a eukaryotic endosymbiont of kinetoplastid ancestry, Perkinsela sp. To investigate the complex relationship between Paramoeba spp. and Perkinsela sp., as well as the relationships between different Paramoeba species, molecular data was obtained for four novel isolates. We also acquired new data from the urchin pathogen P. invadens. Comprehensive molecular phylogenetic analyses were carried out using 33 newly obtained 18S rDNA sequences from the host amoebae and 16 new 18S rDNA sequences from their corresponding Perkinsela sp., together with all publicly available 18S molecular data. Intra-isolate 18S rDNA nucleotide diversity was found to be surprisingly high within the various species of Paramoeba, but relatively low within their Perkinsela sp. endosymbionts. 18S rDNA phylogenies and ParaFit co-evolution analysis revealed a high degree of congruence between the Paramoeba and Perkinsela sp. tree topologies, strongly suggesting that a single endosymbiotic event occurred in the common ancestor of known Paramoeba species, and that the endosymbionts have been inherited vertically ever since.

show abstract

Microheterogeneity and Coevolution: An Examination of rDNA Sequence Characteristics in Neoparamoeba pemaquidensis and Its Prokinetoplastid Endosymbiont

Cited by 28 publications

References 56 publications

Complex etiologies of emerging diseases in lobsters (Homarus americanus) from Long Island Sound

Complex etiologies of emerging diseases in lobsters (Homarus americanus) from Long Island Sound

Genomic Characterization of Neoparamoeba pemaquidensis (Amoebozoa) and Its Kinetoplastid Endosymbiont

Diversity and Evolution of Paramoeba spp. and their Kinetoplastid Endosymbionts

Contact Info

Product

Resources

About