Cultivating the macroalgal holobiont: effects of integrated multi-trophic aquaculture on the microbiome of Ulva rigida (chlorophyta)

Detalhes bibliográficos
Autor(a) principal: Califano, Gianmaria
Data de Publicação: 2020
Outros Autores: Kwantes, Michiel, Abreu, Maria Helena, Da Silva Costa, Rodrigo, Wichard, Thomas
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10400.1/13628
Resumo: Ulva is a ubiquitous macroalgal genus of commercial interest. Integrated Multi-Trophic Aquaculture (IMTA) systems promise large-scale production of macroalgae due to their high productivity and environmental sustainability. Complex host-microbiome interactions play a decisive role in macroalgal development, especially in Ulva spp. due to algal growth- and morphogenesis-promoting factors released by associated bacteria. However, our current understanding of the microbial community assembly and structure in cultivated macroalgae is scant. We aimed to determine (i) to what extent IMTA settings influence the microbiome associated with U. rigida and its rearing water, (ii) to explore the dynamics of beneficial microbes to algal growth and development under IMTA settings, and (iii) to improve current knowledge of host-microbiome interactions. We examined the diversity and taxonomic composition of the prokaryotic communities associated with wild versus IMTA-grown Ulva rigida and surrounding seawater by using 16S rRNA gene amplicon sequencing. With 3141 Amplicon Sequence Variants (ASVs), the prokaryotic richness was, overall, higher in water than in association with U. rigida. Bacterial ASVs were more abundant in aquaculture water samples than water collected from the lagoon. The beta diversity analysis revealed distinct prokaryotic communities associated with Ulva collected in both aquacultures and coastal waters. Aquaculture samples (water and algae) shared 22% of ASVs, whereas natural, coastal lagoon samples only 9%. While cultivated Ulva selected 239 (8%) host-specific ASVs, wild specimens possessed more than twice host-specific ASVs (17%). Cultivated U. rigida specimens enriched the phyla Cyanobacteria, Planctomycetes, Verrucomicrobia, and Proteobacteria. Within the Gammaproteobacteria, while Glaciecola mostly dominated the microbiome in cultivated algae, the genus Granulosicoccus characterized both Ulva microbiomes. In both wild and IMTA settings, the phylum Bacteroidetes was more abundant in the bacterioplankton than in direct association with U. rigida. However, we observed that the Saprospiraceae family within this phylum was barely present in lagoon water but very abundant in aquaculture water. Aquaculture promoted the presence of known morphogenesis-inducing bacteria in water samples. Our study suggests that IMTA significantly shaped the structure and composition of the microbial community of the rearing water and cultivated U. rigida. Detailed analysis revealed the presence of previously undetected taxa associated with Ulva, possessing potentially unknown functional traits.
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spelling Cultivating the macroalgal holobiont: effects of integrated multi-trophic aquaculture on the microbiome of Ulva rigida (chlorophyta)Algal morphogenesisBlue economyGreen algaeHost–microbe interactionsIMTAInfochemicalsMorphogenSea lettuceUlva is a ubiquitous macroalgal genus of commercial interest. Integrated Multi-Trophic Aquaculture (IMTA) systems promise large-scale production of macroalgae due to their high productivity and environmental sustainability. Complex host-microbiome interactions play a decisive role in macroalgal development, especially in Ulva spp. due to algal growth- and morphogenesis-promoting factors released by associated bacteria. However, our current understanding of the microbial community assembly and structure in cultivated macroalgae is scant. We aimed to determine (i) to what extent IMTA settings influence the microbiome associated with U. rigida and its rearing water, (ii) to explore the dynamics of beneficial microbes to algal growth and development under IMTA settings, and (iii) to improve current knowledge of host-microbiome interactions. We examined the diversity and taxonomic composition of the prokaryotic communities associated with wild versus IMTA-grown Ulva rigida and surrounding seawater by using 16S rRNA gene amplicon sequencing. With 3141 Amplicon Sequence Variants (ASVs), the prokaryotic richness was, overall, higher in water than in association with U. rigida. Bacterial ASVs were more abundant in aquaculture water samples than water collected from the lagoon. The beta diversity analysis revealed distinct prokaryotic communities associated with Ulva collected in both aquacultures and coastal waters. Aquaculture samples (water and algae) shared 22% of ASVs, whereas natural, coastal lagoon samples only 9%. While cultivated Ulva selected 239 (8%) host-specific ASVs, wild specimens possessed more than twice host-specific ASVs (17%). Cultivated U. rigida specimens enriched the phyla Cyanobacteria, Planctomycetes, Verrucomicrobia, and Proteobacteria. Within the Gammaproteobacteria, while Glaciecola mostly dominated the microbiome in cultivated algae, the genus Granulosicoccus characterized both Ulva microbiomes. In both wild and IMTA settings, the phylum Bacteroidetes was more abundant in the bacterioplankton than in direct association with U. rigida. However, we observed that the Saprospiraceae family within this phylum was barely present in lagoon water but very abundant in aquaculture water. Aquaculture promoted the presence of known morphogenesis-inducing bacteria in water samples. Our study suggests that IMTA significantly shaped the structure and composition of the microbial community of the rearing water and cultivated U. rigida. Detailed analysis revealed the presence of previously undetected taxa associated with Ulva, possessing potentially unknown functional traits.European Union (EU)642575; German Research Foundation (DFG) CRC 1127 ChemBioSys;COST Action "Phycomorph" FA1406Frontiers MediaSapientiaCalifano, GianmariaKwantes, MichielAbreu, Maria HelenaDa Silva Costa, RodrigoWichard, Thomas2020-03-20T11:26:59Z2020-022020-02-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.1/13628eng2296-7745https://doi.org/10.3389/fmars.2020.00052info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-07-24T10:25:47Zoai:sapientia.ualg.pt:10400.1/13628Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T20:04:46.460143Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv Cultivating the macroalgal holobiont: effects of integrated multi-trophic aquaculture on the microbiome of Ulva rigida (chlorophyta)
title Cultivating the macroalgal holobiont: effects of integrated multi-trophic aquaculture on the microbiome of Ulva rigida (chlorophyta)
spellingShingle Cultivating the macroalgal holobiont: effects of integrated multi-trophic aquaculture on the microbiome of Ulva rigida (chlorophyta)
Califano, Gianmaria
Algal morphogenesis
Blue economy
Green algae
Host–microbe interactions
IMTA
Infochemicals
Morphogen
Sea lettuce
title_short Cultivating the macroalgal holobiont: effects of integrated multi-trophic aquaculture on the microbiome of Ulva rigida (chlorophyta)
title_full Cultivating the macroalgal holobiont: effects of integrated multi-trophic aquaculture on the microbiome of Ulva rigida (chlorophyta)
title_fullStr Cultivating the macroalgal holobiont: effects of integrated multi-trophic aquaculture on the microbiome of Ulva rigida (chlorophyta)
title_full_unstemmed Cultivating the macroalgal holobiont: effects of integrated multi-trophic aquaculture on the microbiome of Ulva rigida (chlorophyta)
title_sort Cultivating the macroalgal holobiont: effects of integrated multi-trophic aquaculture on the microbiome of Ulva rigida (chlorophyta)
author Califano, Gianmaria
author_facet Califano, Gianmaria
Kwantes, Michiel
Abreu, Maria Helena
Da Silva Costa, Rodrigo
Wichard, Thomas
author_role author
author2 Kwantes, Michiel
Abreu, Maria Helena
Da Silva Costa, Rodrigo
Wichard, Thomas
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Sapientia
dc.contributor.author.fl_str_mv Califano, Gianmaria
Kwantes, Michiel
Abreu, Maria Helena
Da Silva Costa, Rodrigo
Wichard, Thomas
dc.subject.por.fl_str_mv Algal morphogenesis
Blue economy
Green algae
Host–microbe interactions
IMTA
Infochemicals
Morphogen
Sea lettuce
topic Algal morphogenesis
Blue economy
Green algae
Host–microbe interactions
IMTA
Infochemicals
Morphogen
Sea lettuce
description Ulva is a ubiquitous macroalgal genus of commercial interest. Integrated Multi-Trophic Aquaculture (IMTA) systems promise large-scale production of macroalgae due to their high productivity and environmental sustainability. Complex host-microbiome interactions play a decisive role in macroalgal development, especially in Ulva spp. due to algal growth- and morphogenesis-promoting factors released by associated bacteria. However, our current understanding of the microbial community assembly and structure in cultivated macroalgae is scant. We aimed to determine (i) to what extent IMTA settings influence the microbiome associated with U. rigida and its rearing water, (ii) to explore the dynamics of beneficial microbes to algal growth and development under IMTA settings, and (iii) to improve current knowledge of host-microbiome interactions. We examined the diversity and taxonomic composition of the prokaryotic communities associated with wild versus IMTA-grown Ulva rigida and surrounding seawater by using 16S rRNA gene amplicon sequencing. With 3141 Amplicon Sequence Variants (ASVs), the prokaryotic richness was, overall, higher in water than in association with U. rigida. Bacterial ASVs were more abundant in aquaculture water samples than water collected from the lagoon. The beta diversity analysis revealed distinct prokaryotic communities associated with Ulva collected in both aquacultures and coastal waters. Aquaculture samples (water and algae) shared 22% of ASVs, whereas natural, coastal lagoon samples only 9%. While cultivated Ulva selected 239 (8%) host-specific ASVs, wild specimens possessed more than twice host-specific ASVs (17%). Cultivated U. rigida specimens enriched the phyla Cyanobacteria, Planctomycetes, Verrucomicrobia, and Proteobacteria. Within the Gammaproteobacteria, while Glaciecola mostly dominated the microbiome in cultivated algae, the genus Granulosicoccus characterized both Ulva microbiomes. In both wild and IMTA settings, the phylum Bacteroidetes was more abundant in the bacterioplankton than in direct association with U. rigida. However, we observed that the Saprospiraceae family within this phylum was barely present in lagoon water but very abundant in aquaculture water. Aquaculture promoted the presence of known morphogenesis-inducing bacteria in water samples. Our study suggests that IMTA significantly shaped the structure and composition of the microbial community of the rearing water and cultivated U. rigida. Detailed analysis revealed the presence of previously undetected taxa associated with Ulva, possessing potentially unknown functional traits.
publishDate 2020
dc.date.none.fl_str_mv 2020-03-20T11:26:59Z
2020-02
2020-02-01T00:00:00Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10400.1/13628
url http://hdl.handle.net/10400.1/13628
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv 2296-7745
https://doi.org/10.3389/fmars.2020.00052
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
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