The transcriptome of the rumen ciliate Entodinium caudatum reveals some of its metabolic features
Abstract Background Rumen ciliates play important roles in rumen function by digesting and fermenting feed and shaping the rumen microbiome. However, they remain poorly understood due to the lack of definitive direct evidence without influence by prokaryotes (including symbionts) in co-cultures or t...
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| Format: | Article |
| Language: | English |
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BMC
2019-12-01
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| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12864-019-6382-x |
| _version_ | 1818610061226803200 |
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| author | Lingling Wang Anas Abu-Doleh Johanna Plank Umit V. Catalyurek Jeffrey L. Firkins Zhongtang Yu |
| author_facet | Lingling Wang Anas Abu-Doleh Johanna Plank Umit V. Catalyurek Jeffrey L. Firkins Zhongtang Yu |
| author_sort | Lingling Wang |
| collection | DOAJ |
| description | Abstract Background Rumen ciliates play important roles in rumen function by digesting and fermenting feed and shaping the rumen microbiome. However, they remain poorly understood due to the lack of definitive direct evidence without influence by prokaryotes (including symbionts) in co-cultures or the rumen. In this study, we used RNA-Seq to characterize the transcriptome of Entodinium caudatum, the most predominant and representative rumen ciliate species. Results Of a large number of transcripts, > 12,000 were annotated to the curated genes in the NR, UniProt, and GO databases. Numerous CAZymes (including lysozyme and chitinase) and peptidases were represented in the transcriptome. This study revealed the ability of E. caudatum to depolymerize starch, hemicellulose, pectin, and the polysaccharides of the bacterial and fungal cell wall, and to degrade proteins. Many signaling pathways, including the ones that have been shown to function in E. caudatum, were represented by many transcripts. The transcriptome also revealed the expression of the genes involved in symbiosis, detoxification of reactive oxygen species, and the electron-transport chain. Overall, the transcriptomic evidence is consistent with some of the previous premises about E. caudatum. However, the identification of specific genes, such as those encoding lysozyme, peptidases, and other enzymes unique to rumen ciliates might be targeted to develop specific and effective inhibitors to improve nitrogen utilization efficiency by controlling the activity and growth of rumen ciliates. The transcriptomic data will also help the assembly and annotation in future genomic sequencing of E. caudatum. Conclusion As the first transcriptome of a single species of rumen ciliates ever sequenced, it provides direct evidence for the substrate spectrum, fermentation pathways, ability to respond to various biotic and abiotic stimuli, and other physiological and ecological features of E. caudatum. The presence and expression of the genes involved in the lysis and degradation of microbial cells highlight the dependence of E. caudatum on engulfment of other rumen microbes for its survival and growth. These genes may be explored in future research to develop targeted control of Entodinium species in the rumen. The transcriptome can also facilitate future genomic studies of E. caudatum and other related rumen ciliates. |
| first_indexed | 2024-12-16T15:08:26Z |
| format | Article |
| id | doaj.art-0e0ebc97c958421cb317730824aa6fd2 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-16T15:08:26Z |
| publishDate | 2019-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-0e0ebc97c958421cb317730824aa6fd22022-12-21T22:27:02ZengBMCBMC Genomics1471-21642019-12-0120111810.1186/s12864-019-6382-xThe transcriptome of the rumen ciliate Entodinium caudatum reveals some of its metabolic featuresLingling Wang0Anas Abu-Doleh1Johanna Plank2Umit V. Catalyurek3Jeffrey L. Firkins4Zhongtang Yu5Department of Animal Sciences, The Ohio State UniversityDepartment of Biomedical Informatics, The Ohio State UniversityDepartment of Animal Sciences, The Ohio State UniversityDepartment of Biomedical Informatics, The Ohio State UniversityDepartment of Animal Sciences, The Ohio State UniversityDepartment of Animal Sciences, The Ohio State UniversityAbstract Background Rumen ciliates play important roles in rumen function by digesting and fermenting feed and shaping the rumen microbiome. However, they remain poorly understood due to the lack of definitive direct evidence without influence by prokaryotes (including symbionts) in co-cultures or the rumen. In this study, we used RNA-Seq to characterize the transcriptome of Entodinium caudatum, the most predominant and representative rumen ciliate species. Results Of a large number of transcripts, > 12,000 were annotated to the curated genes in the NR, UniProt, and GO databases. Numerous CAZymes (including lysozyme and chitinase) and peptidases were represented in the transcriptome. This study revealed the ability of E. caudatum to depolymerize starch, hemicellulose, pectin, and the polysaccharides of the bacterial and fungal cell wall, and to degrade proteins. Many signaling pathways, including the ones that have been shown to function in E. caudatum, were represented by many transcripts. The transcriptome also revealed the expression of the genes involved in symbiosis, detoxification of reactive oxygen species, and the electron-transport chain. Overall, the transcriptomic evidence is consistent with some of the previous premises about E. caudatum. However, the identification of specific genes, such as those encoding lysozyme, peptidases, and other enzymes unique to rumen ciliates might be targeted to develop specific and effective inhibitors to improve nitrogen utilization efficiency by controlling the activity and growth of rumen ciliates. The transcriptomic data will also help the assembly and annotation in future genomic sequencing of E. caudatum. Conclusion As the first transcriptome of a single species of rumen ciliates ever sequenced, it provides direct evidence for the substrate spectrum, fermentation pathways, ability to respond to various biotic and abiotic stimuli, and other physiological and ecological features of E. caudatum. The presence and expression of the genes involved in the lysis and degradation of microbial cells highlight the dependence of E. caudatum on engulfment of other rumen microbes for its survival and growth. These genes may be explored in future research to develop targeted control of Entodinium species in the rumen. The transcriptome can also facilitate future genomic studies of E. caudatum and other related rumen ciliates.https://doi.org/10.1186/s12864-019-6382-xEntodinium caudatumMetabolismRNA-SeqRumen protozoaTranscriptomics |
| spellingShingle | Lingling Wang Anas Abu-Doleh Johanna Plank Umit V. Catalyurek Jeffrey L. Firkins Zhongtang Yu The transcriptome of the rumen ciliate Entodinium caudatum reveals some of its metabolic features BMC Genomics Entodinium caudatum Metabolism RNA-Seq Rumen protozoa Transcriptomics |
| title | The transcriptome of the rumen ciliate Entodinium caudatum reveals some of its metabolic features |
| title_full | The transcriptome of the rumen ciliate Entodinium caudatum reveals some of its metabolic features |
| title_fullStr | The transcriptome of the rumen ciliate Entodinium caudatum reveals some of its metabolic features |
| title_full_unstemmed | The transcriptome of the rumen ciliate Entodinium caudatum reveals some of its metabolic features |
| title_short | The transcriptome of the rumen ciliate Entodinium caudatum reveals some of its metabolic features |
| title_sort | transcriptome of the rumen ciliate entodinium caudatum reveals some of its metabolic features |
| topic | Entodinium caudatum Metabolism RNA-Seq Rumen protozoa Transcriptomics |
| url | https://doi.org/10.1186/s12864-019-6382-x |
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