Spatial Succession Underlies Microbial Contribution to Food Digestion in the Gut of an Algivorous Sea Urchin
ABSTRACT Dietary influence on the microbiome in algivorous sea urchins such as Tripneustes gratilla elatensis suggests a bacterial contribution to the digestion of fiber-rich seaweed. An ecological insight into the spatial arrangement in the gut bacterial community will improve our knowledge of host...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-06-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00514-23 |
| _version_ | 1797803484634939392 |
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| author | Matan Masasa Ariel Kushmaro Dzung Nguyen Helena Chernova Nadav Shashar Lior Guttman |
| author_facet | Matan Masasa Ariel Kushmaro Dzung Nguyen Helena Chernova Nadav Shashar Lior Guttman |
| author_sort | Matan Masasa |
| collection | DOAJ |
| description | ABSTRACT Dietary influence on the microbiome in algivorous sea urchins such as Tripneustes gratilla elatensis suggests a bacterial contribution to the digestion of fiber-rich seaweed. An ecological insight into the spatial arrangement in the gut bacterial community will improve our knowledge of host-microbe relations concerning the involved taxa, their metabolic repertoire, and the niches of activity. Toward this goal, we investigated the bacterial communities in the esophagus, stomach, and intestine of Ulva-fed sea urchins through 16S rRNA amplicon sequencing, followed by the prediction of their functional genes. We revealed communities with distinct features, especially those in the esophagus and intestine. The esophageal community was less diverse and was poor in food digestive or fermentation genes. In contrast, bacteria that can contribute to the digestion of the dietary Ulva were common in the stomach and intestine and consisted of genes for carbohydrate decomposition, fermentation, synthesis of short-chain fatty acids, and various ways of N and S metabolism. Bacteroidetes and Firmicutes were found as the main phyla in the gut and are presumably also necessary in food digestion. The abundant sulfate-reducing bacteria in the stomach and intestine from the genera Desulfotalea, Desulfitispora, and Defluviitalea may aid in removing the excess sulfate from the decomposition of the algal polysaccharides. Although these sea urchins were fed with Ulva, genes for the degradation of polysaccharides of other algae and plants were present in this sea urchin gut microbiome. We conclude that the succession of microbial communities along the gut obtained supports the hypothesis on bacterial contribution to food digestion. IMPORTANCE Alga grazing by the sea urchin Tripneustes gratilla elatensis is vital for nutrient recycling and constructing new reefs. This research was driven by the need to expand the knowledge of bacteria that may aid this host in alga digestion and their phylogeny, roles, and activity niches. We hypothesized alterations in the bacterial compositional structure along the gut and their association with the potential contribution to food digestion. The current spatial insight into the sea urchin’s gut microbiome ecology is novel and reveals how distinct bacterial communities are when distant from each other in this organ. It points to keynote bacteria with genes that may aid the host in the digestion of the complex sulfated polysaccharides in dietary Ulva by removing the released sulfates and fermentation to provide energy. The gut bacteria’s genomic arsenal may also help to gain energy from diets of other algae and plants. |
| first_indexed | 2024-03-13T05:21:37Z |
| format | Article |
| id | doaj.art-bb6439b1498b4e4b99f4d4ef364c9523 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-13T05:21:37Z |
| publishDate | 2023-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-bb6439b1498b4e4b99f4d4ef364c95232023-06-15T13:18:31ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.00514-23Spatial Succession Underlies Microbial Contribution to Food Digestion in the Gut of an Algivorous Sea UrchinMatan Masasa0Ariel Kushmaro1Dzung Nguyen2Helena Chernova3Nadav Shashar4Lior Guttman5Marine Biology and Biotechnology Program, Department of Life Sciences, Ben-Gurion University of the Negev, Eilat, IsraelAvram and Stella Goldstein-Goren Department of Biotechnology Engineering, Ben-Gurion University of the Negev, Beer-Sheva, IsraelMarine Biology and Biotechnology Program, Department of Life Sciences, Ben-Gurion University of the Negev, Eilat, IsraelIsrael Oceanographic and Limnological Research, The National Center for Mariculture, Eilat, IsraelMarine Biology and Biotechnology Program, Department of Life Sciences, Ben-Gurion University of the Negev, Eilat, IsraelIsrael Oceanographic and Limnological Research, The National Center for Mariculture, Eilat, IsraelABSTRACT Dietary influence on the microbiome in algivorous sea urchins such as Tripneustes gratilla elatensis suggests a bacterial contribution to the digestion of fiber-rich seaweed. An ecological insight into the spatial arrangement in the gut bacterial community will improve our knowledge of host-microbe relations concerning the involved taxa, their metabolic repertoire, and the niches of activity. Toward this goal, we investigated the bacterial communities in the esophagus, stomach, and intestine of Ulva-fed sea urchins through 16S rRNA amplicon sequencing, followed by the prediction of their functional genes. We revealed communities with distinct features, especially those in the esophagus and intestine. The esophageal community was less diverse and was poor in food digestive or fermentation genes. In contrast, bacteria that can contribute to the digestion of the dietary Ulva were common in the stomach and intestine and consisted of genes for carbohydrate decomposition, fermentation, synthesis of short-chain fatty acids, and various ways of N and S metabolism. Bacteroidetes and Firmicutes were found as the main phyla in the gut and are presumably also necessary in food digestion. The abundant sulfate-reducing bacteria in the stomach and intestine from the genera Desulfotalea, Desulfitispora, and Defluviitalea may aid in removing the excess sulfate from the decomposition of the algal polysaccharides. Although these sea urchins were fed with Ulva, genes for the degradation of polysaccharides of other algae and plants were present in this sea urchin gut microbiome. We conclude that the succession of microbial communities along the gut obtained supports the hypothesis on bacterial contribution to food digestion. IMPORTANCE Alga grazing by the sea urchin Tripneustes gratilla elatensis is vital for nutrient recycling and constructing new reefs. This research was driven by the need to expand the knowledge of bacteria that may aid this host in alga digestion and their phylogeny, roles, and activity niches. We hypothesized alterations in the bacterial compositional structure along the gut and their association with the potential contribution to food digestion. The current spatial insight into the sea urchin’s gut microbiome ecology is novel and reveals how distinct bacterial communities are when distant from each other in this organ. It points to keynote bacteria with genes that may aid the host in the digestion of the complex sulfated polysaccharides in dietary Ulva by removing the released sulfates and fermentation to provide energy. The gut bacteria’s genomic arsenal may also help to gain energy from diets of other algae and plants.https://journals.asm.org/doi/10.1128/spectrum.00514-23gut microbiomehost-bacterium associationsmicrobial ecologyniche specificationalgal dietmetabolism |
| spellingShingle | Matan Masasa Ariel Kushmaro Dzung Nguyen Helena Chernova Nadav Shashar Lior Guttman Spatial Succession Underlies Microbial Contribution to Food Digestion in the Gut of an Algivorous Sea Urchin Microbiology Spectrum gut microbiome host-bacterium associations microbial ecology niche specification algal diet metabolism |
| title | Spatial Succession Underlies Microbial Contribution to Food Digestion in the Gut of an Algivorous Sea Urchin |
| title_full | Spatial Succession Underlies Microbial Contribution to Food Digestion in the Gut of an Algivorous Sea Urchin |
| title_fullStr | Spatial Succession Underlies Microbial Contribution to Food Digestion in the Gut of an Algivorous Sea Urchin |
| title_full_unstemmed | Spatial Succession Underlies Microbial Contribution to Food Digestion in the Gut of an Algivorous Sea Urchin |
| title_short | Spatial Succession Underlies Microbial Contribution to Food Digestion in the Gut of an Algivorous Sea Urchin |
| title_sort | spatial succession underlies microbial contribution to food digestion in the gut of an algivorous sea urchin |
| topic | gut microbiome host-bacterium associations microbial ecology niche specification algal diet metabolism |
| url | https://journals.asm.org/doi/10.1128/spectrum.00514-23 |
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