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Marine Biotechnology

, Volume 16, Issue 1, pp 17–33 | Cite as

Transcriptome Analysis Reveals a Rich Gene Set Related to Innate Immunity in the Eastern Oyster (Crassostrea virginica)

  • Linlin Zhang
  • Li Li
  • Yabing Zhu
  • Guofan Zhang
  • Ximing Guo
Original Article

Abstract

As a benthic filter-feeder of estuaries, the eastern oyster, Crassostrea virginica, faces tremendous exposure to microbial pathogens. How eastern oysters without adaptive immunity survive in pathogen-rich environments is of fundamental interest, but studies on its immune system are hindered by the lack of genomic resources. We sequenced the transcriptome of an adult oyster with short Illumina reads and assembled 66,229 contigs with a N50 length of 1,503 bp. The assembly covered 89.4 % of published ESTs and 97.9 % of mitochondrial genes demonstrating its quality. A set of 39,978 contigs and unigenes (>300 bp) were identified and annotated by searching public databases. Analysis of the gene set yielded a diverse set of 657 genes related to innate immunity, including many pertaining to pattern recognition, effectors, signal transduction, cytokines, and apoptosis. Gene families encoding C1q domain containing proteins, CTLD, IAPs, Ig_I-set, and TRAFs expanded in C. virginica and Crassostrea gigas. Many key genes of the apoptosis system including IAP, BAX, BAC-2, caspase, FADD, and TNFR were identified, suggesting C. virginica posses advanced apoptosis and apoptosis-regulating systems. Our results show that short Illumina reads can produce transcriptomes of highly polymorphic genomes with coverage and integrity comparable to that from longer 454 reads. The expansion and high diversity in gene families related to innate immunity, point to a complex defense system in the lophotrochozoan C. virginica, probably in adaptation to a pathogen-rich environment.

Keywords

Innate immunity Apoptosis Transcriptome Disease Adaptation Mollusca 

Abbreviations

TLR

Toll-like receptor

SRCR

Scavenger domain containing protein

CD36-like

Cluster of differentiation 36 like gene

PGRP

Peptidoglycan recognition protein

GNBP

Gram-negative binding protein

CTLD

C type lectin domain containing protein

C1qDC

C1q domain containing protein

NOS

Nitric oxide synthase

BPI

Bactericidal permeability-increasing protein

SOD

Superoxide dismutase

IKK

IκB kinase

Rel/NF-κB

Rel or nuclear factor kappa B

TBK

Serine/threonine-protein kinase TBK1

TRAF

TNF receptor-associated factor

IRAK

Interleukin-1 receptor-associated kinase

TRIAD

E3 ubiquitin-protein ligase ARIH

MyD88

Myeloid differentiation primary response gene (88)

SARM

Sterile alpha and TIR motif-containing protein

MIF

Macrophage migration inhibitory factor

TNF

Tumor necrosis factor

TNFR

Tumor necrosis factor receptor

FADD

FAS-associated death domain protein

IAP

Inhibitor of apoptosis protein

Bcl-2

Apoptosis regulator Bcl-2

Bax

Apoptosis regulator Bax

Notes

Acknowledgments

We thank Laodong Aquaculture Breeding Company for providing oysters. Thanks also to Ping Zhang, Zengfang Zhao in high-performance computing center of Institute of Oceanology, CAS, for providing computing resources. This research was supported in part by National Basic Research Program of China (973 Program, No. 2010CB126401), National High Technology Research and Development Program (863 program, 2012AA10A405), the National Natural Science Foundation of China (no. 40730845), Molluscan Research and Development Center, CARS, Taishan Scholars Climbing Program of Shandong and Taishan Oversea Scholar Program of Shandong, US NSF EID award (OCE-0622672), and RAPID award (OCE-1136530).

Supplementary material

10126_2013_9526_MOESM1_ESM.doc (51 kb)
Supplementary file 1 Cross-mapping statistics among different assemblies of Crassostrea virginica transcriptome. (DOC 51 kb)
10126_2013_9526_MOESM2_ESM.doc (35 kb)
Supplementary file 2 Mapping of assembled contigs with BLASTN against the 12 Crassostrea virginica mitochondrial protein coding genes at a cut-off E value of 1E-5. (DOC 35 kb)
10126_2013_9526_MOESM3_ESM.doc (30 kb)
Supplementary file 3 Simple sequence repeats (SSRs) identified in the transcriptome of Crassostrea virginica. (DOC 30 kb)
10126_2013_9526_MOESM4_ESM.txt (2.2 mb)
Supplementary file 4 Annotation by top hits from BLASTX of Crassostrea virginica unigenes against the nr protein database with a cut-off E value of 1E-5. (TXT 2231 kb)
10126_2013_9526_MOESM5_ESM.fa (11.1 mb)
Supplementary file 5 Crassostrea virginica transcriptome protein set based on the Oases k-mer 23 assembly. Only proteins longer than 100 amino acids are included. (FA 11414 kb)
10126_2013_9526_MOESM6_ESM.txt (4.6 mb)
Supplementary file 6 InterProScan annotation of predicted Crassostrea virginica genes. (TXT 4688 kb)
10126_2013_9526_MOESM7_ESM.txt (5.2 mb)
Supplementary file 7 GO annotation of predicted Crassostrea virginica genes. (TXT 5304 kb)
10126_2013_9526_MOESM8_ESM.txt (1.5 mb)
Supplementary file 8 KEGG pathway mapping of Crassostrea virginica genes. (TXT 1508 kb)
10126_2013_9526_MOESM9_ESM.doc (94 kb)
Supplementary file 9 Complete list of immunity-related unigenes found in Crassostrea virginica transcriptome (with predicted unigene IDs). (DOC 94 kb)

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Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Institute of OceanologyChinese Academy of SciencesQingdaoChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.BGI-ShenzhenShenzhenChina
  4. 4.Haskin Shellfish Research Laboratory, Institute of Marine and Coastal SciencesRutgers UniversityPort NorrisUSA

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