Niche–dependent sponge hologenome expression profiles and the host-microbes interplay: a case of the hawaiian demosponge Mycale Grandis

Abstract Background Most researches on sponge holobionts focus primarily on symbiotic microbes, yet data at the level of the sponge hologenome are still relatively scarce. Understanding of the sponge host and its microbial gene expression profiles and the host-microbes interplay in different niches...

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Main Authors: Fang Liu, Taewoo Ryu, Timothy Ravasi, Xin Wang, Guangyi Wang, Zhiyong Li
Format: Article
Language:English
Published: BMC 2024-04-01
Series:Environmental Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s40793-024-00563-8
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author Fang Liu
Taewoo Ryu
Timothy Ravasi
Xin Wang
Guangyi Wang
Zhiyong Li
author_facet Fang Liu
Taewoo Ryu
Timothy Ravasi
Xin Wang
Guangyi Wang
Zhiyong Li
author_sort Fang Liu
collection DOAJ
description Abstract Background Most researches on sponge holobionts focus primarily on symbiotic microbes, yet data at the level of the sponge hologenome are still relatively scarce. Understanding of the sponge host and its microbial gene expression profiles and the host-microbes interplay in different niches represents a key aspect of sponge hologenome. Using the Hawaiian demosponge Mycale grandis in different niches as a model, i.e. on rocks, on the surface of coral Porites compressa, under alga Gracilaria salicornia, we compared the bacterial and fungal community structure, functional gene diversity, expression pattern and the host transcriptome by integrating open-format (deep sequencing) and closed-format (GeoChip microarray) high-throughput techniques. Results Little inter-niche variation in bacterial and fungal phylogenetic diversity was detected for M. grandis in different niches, but a clear niche-dependent variability in the functional gene diversity and expression pattern of M. grandis host and its symbiotic microbiota was uncovered by GeoChip microarray and transcriptome analyses. Particularly, sponge host genes related to innate immunity and microbial recognition showed a strong correlation with the microbial symbionts’ functional gene diversity and transcriptional richness in different niches. The cross-niche variability with respect to the symbiont functional gene diversity and the transcriptional richness of M. grandis holobiont putatively reflects the interplay of niche-specific selective pressure and the symbiont functional diversity. Conclusions Niche–dependent gene expression profiles of M. grandis hologenome and the host-microbes interplay were suggested though little inter-niche variation in bacterial and fungal diversity was detected, particularly the sponge innate immunity was found to be closely related to the symbiotic microbes. Altogether, these findings provide novel insights into the black box of one sponge holobiont in different niches at the hologenome level.
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spelling doaj.art-c8449a8342f94b90a77b9a351242da542024-04-14T11:29:51ZengBMCEnvironmental Microbiome2524-63722024-04-0119111510.1186/s40793-024-00563-8Niche–dependent sponge hologenome expression profiles and the host-microbes interplay: a case of the hawaiian demosponge Mycale GrandisFang Liu0Taewoo Ryu1Timothy Ravasi2Xin Wang3Guangyi Wang4Zhiyong Li5State Key Laboratory of Microbial Metabolism, School of Life Sciences & Biotechnology, Shanghai Jiao Tong UniversityMarine Climate Change Unit, Okinawa Institute of Science and Technology Graduate University (OIST), 1919-1 Tancha, Onna-sonMarine Climate Change Unit, Okinawa Institute of Science and Technology Graduate University (OIST), 1919-1 Tancha, Onna-sonDepartment of Microbiology and Cell Science, Institute of Food and Agricultural Sciences, University of FloridaSchool of Environmental Science and Engineering, Tianjin UniversityState Key Laboratory of Microbial Metabolism, School of Life Sciences & Biotechnology, Shanghai Jiao Tong UniversityAbstract Background Most researches on sponge holobionts focus primarily on symbiotic microbes, yet data at the level of the sponge hologenome are still relatively scarce. Understanding of the sponge host and its microbial gene expression profiles and the host-microbes interplay in different niches represents a key aspect of sponge hologenome. Using the Hawaiian demosponge Mycale grandis in different niches as a model, i.e. on rocks, on the surface of coral Porites compressa, under alga Gracilaria salicornia, we compared the bacterial and fungal community structure, functional gene diversity, expression pattern and the host transcriptome by integrating open-format (deep sequencing) and closed-format (GeoChip microarray) high-throughput techniques. Results Little inter-niche variation in bacterial and fungal phylogenetic diversity was detected for M. grandis in different niches, but a clear niche-dependent variability in the functional gene diversity and expression pattern of M. grandis host and its symbiotic microbiota was uncovered by GeoChip microarray and transcriptome analyses. Particularly, sponge host genes related to innate immunity and microbial recognition showed a strong correlation with the microbial symbionts’ functional gene diversity and transcriptional richness in different niches. The cross-niche variability with respect to the symbiont functional gene diversity and the transcriptional richness of M. grandis holobiont putatively reflects the interplay of niche-specific selective pressure and the symbiont functional diversity. Conclusions Niche–dependent gene expression profiles of M. grandis hologenome and the host-microbes interplay were suggested though little inter-niche variation in bacterial and fungal diversity was detected, particularly the sponge innate immunity was found to be closely related to the symbiotic microbes. Altogether, these findings provide novel insights into the black box of one sponge holobiont in different niches at the hologenome level.https://doi.org/10.1186/s40793-024-00563-8Mycale GrandisHologenomeGene expressionHost-microbe interplay(Meta)transcriptomeGeoChip microarray
spellingShingle Fang Liu
Taewoo Ryu
Timothy Ravasi
Xin Wang
Guangyi Wang
Zhiyong Li
Niche–dependent sponge hologenome expression profiles and the host-microbes interplay: a case of the hawaiian demosponge Mycale Grandis
Environmental Microbiome
Mycale Grandis
Hologenome
Gene expression
Host-microbe interplay
(Meta)transcriptome
GeoChip microarray
title Niche–dependent sponge hologenome expression profiles and the host-microbes interplay: a case of the hawaiian demosponge Mycale Grandis
title_full Niche–dependent sponge hologenome expression profiles and the host-microbes interplay: a case of the hawaiian demosponge Mycale Grandis
title_fullStr Niche–dependent sponge hologenome expression profiles and the host-microbes interplay: a case of the hawaiian demosponge Mycale Grandis
title_full_unstemmed Niche–dependent sponge hologenome expression profiles and the host-microbes interplay: a case of the hawaiian demosponge Mycale Grandis
title_short Niche–dependent sponge hologenome expression profiles and the host-microbes interplay: a case of the hawaiian demosponge Mycale Grandis
title_sort niche dependent sponge hologenome expression profiles and the host microbes interplay a case of the hawaiian demosponge mycale grandis
topic Mycale Grandis
Hologenome
Gene expression
Host-microbe interplay
(Meta)transcriptome
GeoChip microarray
url https://doi.org/10.1186/s40793-024-00563-8
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