Integrated transcriptomics and proteomics analysis reveals muscle metabolism effects of dietary Ulva lactuca and ulvan lyase supplementation in weaned piglets
Abstract Seaweeds, including the green Ulva lactuca, can potentially reduce competition between feed, food, and fuel. They can also contribute to the improved development of weaned piglets. However, their indigestible polysaccharides of the cell wall pose a challenge. This can be addressed through c...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2024-02-01
|
| Series: | Scientific Reports |
| Subjects: | |
| Online Access: | https://doi.org/10.1038/s41598-024-55462-2 |
| _version_ | 1797274488134434816 |
|---|---|
| author | David Miguel Ribeiro Diogo Coelho Mónica Costa Daniela Filipa Pires Carvalho Céline C. Leclercq Jenny Renaut João Pedro Bengala Freire André Martinho Almeida José António Mestre Prates |
| author_facet | David Miguel Ribeiro Diogo Coelho Mónica Costa Daniela Filipa Pires Carvalho Céline C. Leclercq Jenny Renaut João Pedro Bengala Freire André Martinho Almeida José António Mestre Prates |
| author_sort | David Miguel Ribeiro |
| collection | DOAJ |
| description | Abstract Seaweeds, including the green Ulva lactuca, can potentially reduce competition between feed, food, and fuel. They can also contribute to the improved development of weaned piglets. However, their indigestible polysaccharides of the cell wall pose a challenge. This can be addressed through carbohydrase supplementation, such as the recombinant ulvan lyase. The objective of our study was to assess the muscle metabolism of weaned piglets fed with 7% U. lactuca and 0.01% ulvan lyase supplementation, using an integrated transcriptomics (RNA-seq) and proteomics (LC–MS) approach. Feeding piglets with seaweed and enzyme supplementation resulted in reduced macronutrient availability, leading to protein degradation through the proteasome (PSMD2), with resulting amino acids being utilized as an energy source (GOT2, IDH3B). Moreover, mineral element accumulation may have contributed to increased oxidative stress, evident from elevated levels of antioxidant proteins like catalase, as a response to maintaining tissue homeostasis. The upregulation of the gene AQP7, associated with the osmotic stress response, further supports these findings. Consequently, an increase in chaperone activity, including HSP90, was required to repair damaged proteins. Our results suggest that enzymatic supplementation may exacerbate the effects observed from feeding U. lactuca alone, potentially due to side effects of cell wall degradation during digestion. |
| first_indexed | 2024-03-07T15:00:03Z |
| format | Article |
| id | doaj.art-0cda13a4305643498bf8a8ea4e2ddf3e |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-07T15:00:03Z |
| publishDate | 2024-02-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-0cda13a4305643498bf8a8ea4e2ddf3e2024-03-05T19:11:29ZengNature PortfolioScientific Reports2045-23222024-02-0114111510.1038/s41598-024-55462-2Integrated transcriptomics and proteomics analysis reveals muscle metabolism effects of dietary Ulva lactuca and ulvan lyase supplementation in weaned pigletsDavid Miguel Ribeiro0Diogo Coelho1Mónica Costa2Daniela Filipa Pires Carvalho3Céline C. Leclercq4Jenny Renaut5João Pedro Bengala Freire6André Martinho Almeida7José António Mestre Prates8Associate Laboratory TERRA, LEAF - Linking Landscape, Environment, Agriculture and Food Research Centre, Instituto Superior de Agronomia, Universidade de LisboaFaculdade de Medicina Veterinária, CIISA - Centre for Interdisciplinary Research in Animal Health, Universidade de LisboaFaculdade de Medicina Veterinária, CIISA - Centre for Interdisciplinary Research in Animal Health, Universidade de LisboaAssociate Laboratory TERRA, LEAF - Linking Landscape, Environment, Agriculture and Food Research Centre, Instituto Superior de Agronomia, Universidade de LisboaBiotechnology Environmental Analysis Platform (BEAP), Environmental Research and Innovation Department (ERIN), LIST- Luxembourg Institute of Science and TechnologyBiotechnology Environmental Analysis Platform (BEAP), Environmental Research and Innovation Department (ERIN), LIST- Luxembourg Institute of Science and TechnologyAssociate Laboratory TERRA, LEAF - Linking Landscape, Environment, Agriculture and Food Research Centre, Instituto Superior de Agronomia, Universidade de LisboaAssociate Laboratory TERRA, LEAF - Linking Landscape, Environment, Agriculture and Food Research Centre, Instituto Superior de Agronomia, Universidade de LisboaFaculdade de Medicina Veterinária, CIISA - Centre for Interdisciplinary Research in Animal Health, Universidade de LisboaAbstract Seaweeds, including the green Ulva lactuca, can potentially reduce competition between feed, food, and fuel. They can also contribute to the improved development of weaned piglets. However, their indigestible polysaccharides of the cell wall pose a challenge. This can be addressed through carbohydrase supplementation, such as the recombinant ulvan lyase. The objective of our study was to assess the muscle metabolism of weaned piglets fed with 7% U. lactuca and 0.01% ulvan lyase supplementation, using an integrated transcriptomics (RNA-seq) and proteomics (LC–MS) approach. Feeding piglets with seaweed and enzyme supplementation resulted in reduced macronutrient availability, leading to protein degradation through the proteasome (PSMD2), with resulting amino acids being utilized as an energy source (GOT2, IDH3B). Moreover, mineral element accumulation may have contributed to increased oxidative stress, evident from elevated levels of antioxidant proteins like catalase, as a response to maintaining tissue homeostasis. The upregulation of the gene AQP7, associated with the osmotic stress response, further supports these findings. Consequently, an increase in chaperone activity, including HSP90, was required to repair damaged proteins. Our results suggest that enzymatic supplementation may exacerbate the effects observed from feeding U. lactuca alone, potentially due to side effects of cell wall degradation during digestion.https://doi.org/10.1038/s41598-024-55462-2Weaned pigletUlva lactucaMuscleTranscriptomicsProteomics |
| spellingShingle | David Miguel Ribeiro Diogo Coelho Mónica Costa Daniela Filipa Pires Carvalho Céline C. Leclercq Jenny Renaut João Pedro Bengala Freire André Martinho Almeida José António Mestre Prates Integrated transcriptomics and proteomics analysis reveals muscle metabolism effects of dietary Ulva lactuca and ulvan lyase supplementation in weaned piglets Scientific Reports Weaned piglet Ulva lactuca Muscle Transcriptomics Proteomics |
| title | Integrated transcriptomics and proteomics analysis reveals muscle metabolism effects of dietary Ulva lactuca and ulvan lyase supplementation in weaned piglets |
| title_full | Integrated transcriptomics and proteomics analysis reveals muscle metabolism effects of dietary Ulva lactuca and ulvan lyase supplementation in weaned piglets |
| title_fullStr | Integrated transcriptomics and proteomics analysis reveals muscle metabolism effects of dietary Ulva lactuca and ulvan lyase supplementation in weaned piglets |
| title_full_unstemmed | Integrated transcriptomics and proteomics analysis reveals muscle metabolism effects of dietary Ulva lactuca and ulvan lyase supplementation in weaned piglets |
| title_short | Integrated transcriptomics and proteomics analysis reveals muscle metabolism effects of dietary Ulva lactuca and ulvan lyase supplementation in weaned piglets |
| title_sort | integrated transcriptomics and proteomics analysis reveals muscle metabolism effects of dietary ulva lactuca and ulvan lyase supplementation in weaned piglets |
| topic | Weaned piglet Ulva lactuca Muscle Transcriptomics Proteomics |
| url | https://doi.org/10.1038/s41598-024-55462-2 |
| work_keys_str_mv | AT davidmiguelribeiro integratedtranscriptomicsandproteomicsanalysisrevealsmusclemetabolismeffectsofdietaryulvalactucaandulvanlyasesupplementationinweanedpiglets AT diogocoelho integratedtranscriptomicsandproteomicsanalysisrevealsmusclemetabolismeffectsofdietaryulvalactucaandulvanlyasesupplementationinweanedpiglets AT monicacosta integratedtranscriptomicsandproteomicsanalysisrevealsmusclemetabolismeffectsofdietaryulvalactucaandulvanlyasesupplementationinweanedpiglets AT danielafilipapirescarvalho integratedtranscriptomicsandproteomicsanalysisrevealsmusclemetabolismeffectsofdietaryulvalactucaandulvanlyasesupplementationinweanedpiglets AT celinecleclercq integratedtranscriptomicsandproteomicsanalysisrevealsmusclemetabolismeffectsofdietaryulvalactucaandulvanlyasesupplementationinweanedpiglets AT jennyrenaut integratedtranscriptomicsandproteomicsanalysisrevealsmusclemetabolismeffectsofdietaryulvalactucaandulvanlyasesupplementationinweanedpiglets AT joaopedrobengalafreire integratedtranscriptomicsandproteomicsanalysisrevealsmusclemetabolismeffectsofdietaryulvalactucaandulvanlyasesupplementationinweanedpiglets AT andremartinhoalmeida integratedtranscriptomicsandproteomicsanalysisrevealsmusclemetabolismeffectsofdietaryulvalactucaandulvanlyasesupplementationinweanedpiglets AT joseantoniomestreprates integratedtranscriptomicsandproteomicsanalysisrevealsmusclemetabolismeffectsofdietaryulvalactucaandulvanlyasesupplementationinweanedpiglets |