Alterations of the immune transcriptome in resistant and susceptible hard clams (Mercenaria mercenaria) in response to Quahog Parasite Unknown (QPX) and temperature

Wang, Kailai; Espinosa, Emmanuelle Pales; Tanguy, Arnaud; Allam, Bassem

doi:10.1016/j.fsi.2015.12.006

Cited by 21 publications

(12 citation statements)

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“…Temperature has profound effects on the transcriptional activity of organisms, from prokaryotes (Smoot et al, ), plants (Winfield, Lu, Wilson, Coghill, & Edwards, ), fungi (Steen et al, ), invertebrates (Wang, Espinosa, Tanguy., & Allam, ) to vertebrates (Gracey et al, ). In multicellular organisms, temperature‐dependent gene expression responses are often tissue‐specific (Gracey et al, ).…”

Section: Introductionmentioning

confidence: 99%

Temperature‐mediated shifts in salamander transcriptomic responses to the amphibian‐killing fungus

et al. 2020

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Life processes of ectothermic vertebrates are intimately linked to the temperature of their environment, influencing their metabolism, reproduction, behaviour and immune responses. In amphibians infected by the generalist chytrid pathogen Batrachochytrium dendrobatidis (Bd), host survival, infection prevalence and infection intensity are often temperature‐ and/or seasonally dependent. However, the transcriptional underpinnings of thermal differences in infection responses remain unknown. Measuring the impact of temperature on host responses to infection is a key component for understanding climatic influences on chytrid disease dynamics. The Bd‐responsive gene pathways in frogs are well documented, but our understanding of salamander immune expression profiles during infection with chytrids remains limited. Here we characterize the transcriptomic responses of Plethodon cinereus using RNA sequencing by comparing skin and splenic gene expression of individuals uninfected, succumbing to Bd infection and naturally cleared of Bd infection at three temperatures. We suggest that amphibian temperature‐dependent susceptibility to Bd is probably driven by shifts in expression of the innate and adaptive immune axes. Our study shows increased expression of transcripts associated with inflammation at lower temperatures and a shift towards increased expression of adaptive immune genes, including MHC (major histocompatibility complex), at higher temperatures. In the face of climate change, and as concerns for the spread of emergent chytrid pathogens increase, our results provide important functional genomic resources to help understand how these pathogenic fungi may continue to affect amphibian communities globally in the future.

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Section: Introductionmentioning

confidence: 99%

Temperature‐mediated shifts in salamander transcriptomic responses to the amphibian‐killing fungus

et al. 2020

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“…Additionally, prior work showed that environmental factors affected host fitness and immune performances leading to enhanced susceptibility or, alternatively, resistance to QPX [ 3 , 4 , 6 , 45 ]. For example, disease prevalence and intensity were markedly higher in clams exposed to low temperatures (13 °C) as compared to animals held at milder temperatures (21 °C and 27 °C) [ 46 ].…”

Section: Resultsmentioning

confidence: 99%

SNP hot-spots in the clam parasite QPX

Bassim

Allam

2018

BMC Genomics

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BackgroundQuahog Parasite Unknown (QPX) is an opportunistic protistan pathogen of the clam Mercenaria mercenaria. Infections with QPX have caused significant economic losses in the Northeastern United States. Previous research demonstrated a geographic gradient for disease prevalence and intensity, but little information is available on the genetic diversity of the parasite throughout its distribution range. Also, QPX virulence factors are not well understood. This study addresses the occurrence of QPX genetic variants with a particular focus on functions involved in virulence and adaptation to environmental conditions.ResultsAnalyses were performed using transcriptome-wide single-nucleotide polymorphism (SNP) of four QPX isolates cultured from infected clams collected from disparate locations along the Northeastern United States. For contig assembly and mapping, two different genome builds and four transcriptomes of the parasite were examined. Genomic variants appeared at a differential rate relative to sequenced transcripts at 20.18 and 22.55% occurrence under 1000 base pairs upstream and downstream protein domains respectively and at 57.26% rate in protein domain coding sequences. QPX strains shared 30.50% of the mutations and exhibited a preferential nucleotide substitution towards thymine. Sequence identity suggested relatedness between different QPX strains, with the parasite being possibly introduced to Virginia from the Massachusetts region during clam trading, while QPX could have been naturally present in New York. Diversity in virulence, temperature, and salinity domains suggested a common variability between strains, but with a preferential higher variation in local adaptation genes. This could explain differences in disease prevalence noted in different regions. Overall, the results supported views that this opportunistic parasite might be able to adapt to varying environmental conditions.ConclusionRelatedness and mutations between the four QPX strains suggested that variability in environmental-related functions favors parasite survival, potentially promoting resilience against stressful conditions. These findings are in agreement with the widespread presence of QPX in the environment. Although QPX levels are enzootic in most areas, an increase in disease outbreaks were often associated with seasonal changes in environmental conditions. A selection mediated by the parasitic life of QPX remains possible, but the effect of the environment on the biology of the parasite appears more obvious.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4866-8) contains supplementary material, which is available to authorized users.

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“…Expansion of complement, redox, chaperone, and protein recycling enzyme families across bivalves is thought to have occurred in a species-specific manner ( Wang et al 2010 , 2016 ; Fleury and Huvet 2012 ; Takeuchi et al 2016 ). We found evidence of conserved ancestral duplication (retained by >66% of bivalves) among four gene families (OG92, OG10, OG53, OG314, and OG1538) ( table 1 ).…”

Section: Main Textmentioning

confidence: 99%

Ancestral Physical Stress and Later Immune Gene Family Expansions Shaped Bivalve Mollusc Evolution

Regan

Stevens

Peñaloza

et al. 2021

Genome Biology and Evolution

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Bivalve molluscs comprise 20,000 species occupying a wide diversity of marine habitats. As filter feeders and detritivores they act as ecosystem engineers clarifying water, creating reefs and protecting coastlines. The global decline of natural oyster reefs has led to increased restoration efforts in recent years. Bivalves also play an important role in global food security contributing to > 20% of worldwide aquaculture production. Despite this importance, relatively little is known about bivalve evolutionary adaptation strategies. Difficulties previously associated with highly heterozygous and repetitive regions of bivalve genomes have been overcome by long read sequencing, enabling the generation of accurate bivalve assemblies. With these resources we have analysed the genomes of 32 species representing each molluscan class, including 15 bivalve species, to identify gene families that have undergone expansion during bivalve evolution. Gene family expansions across bivalve genomes occur at the point of evolutionary pressures. We uncovered two key factors that shape bivalve evolutionary history: expansion of bivalvia into environmental niches with high stress followed by later exposure to specific pathogenic pressures. The conserved expansion of protein recycling gene families we found across bivalvia is mirrored by adaptations to a sedentary lifestyle seen in plants. These results reflect the ability of bivalves to tolerate high levels of environmental stress and constant exposure to pathogens as filter feeders. The increasing availability of accurate genome assemblies will provide greater resolution to these analyses allowing further points of evolutionary pressure to become clear in other understudied taxa and potentially different populations of a single species.

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Alterations of the immune transcriptome in resistant and susceptible hard clams (Mercenaria mercenaria) in response to Quahog Parasite Unknown (QPX) and temperature

Cited by 21 publications

References 76 publications

Temperature‐mediated shifts in salamander transcriptomic responses to the amphibian‐killing fungus

Temperature‐mediated shifts in salamander transcriptomic responses to the amphibian‐killing fungus

SNP hot-spots in the clam parasite QPX

Ancestral Physical Stress and Later Immune Gene Family Expansions Shaped Bivalve Mollusc Evolution

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