Sea urchin microbiomes vary with habitat and resource availability

Miller, Paige M.; Lamy, Thomas; Page, Henry M.; Miller, Robert J.

doi:10.1002/lol2.10189

Cited by 7 publications

(11 citation statements)

References 36 publications

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“…Psychromonas sp. has also been detected in S. purpuratus (Hakim et al 2019;Miller et al 2021) and S. intermedius (Zhang et al 2014) and was abundant especially in gut digesta and fecal pellets, analogous to our sample material. Thus, this symbiont appears to be a common feature of the intestinal microbiome of sea urchins belonging to the Strongylocentrotus genus, which could point towards important symbiotic functions.…”

Section: Algal Food Intake Promotes a Dominant Symbiont Related To Ps...supporting

confidence: 82%

The sea urchin intestinal microbiome responds dynamically to food intake and contains nitrogen-fixing symbionts

Bengtsson,

Helgesen,

Wang

et al. 2024

Preprint

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Kelp deforestation by sea urchin grazing is a widespread phenomenon globally, with vast consequences for coastal ecosystems. The ability of sea urchins to survive on a kelp diet of poor nutritional quality is not well understood and bacterial communities in the sea urchin intestine may play an important role in digestion. A no-choice feeding experiment was conducted with the sea urchinStrongylocentrotus droebachiensis, offering three different seaweeds as diet, including the kelpSaccharina latissima. Starved sea urchins served as experimental control. Amplicons of the 16S rRNA gene were analyzed from fecal pellets. One dominant symbiont (Psychromonas marina) accounted for 44 % of all sequence reads and was especially abundant in the sea urchins fed seaweed diets. The starved and field captured sea urchins consistently displayed higher diversity than the seaweed-fed sea urchins and displayed a higher predicted abundance of genes involved in nitrogen fixation. Cloning and sequencing of the NifH gene revealed diverse nitrogen fixers. We demonstrate that the sea urchin intestinal microbiome is dynamic, responds to diet and has the capacity for nitrogen fixation. The microbiome thereby reflects the dietary flexibility of these sea urchins, and could be a key component in understanding catastrophic kelp forest grazing events.

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Section: Algal Food Intake Promotes a Dominant Symbiont Related To Ps...supporting

confidence: 82%

The sea urchin intestinal microbiome responds dynamically to food intake and contains nitrogen-fixing symbionts

Bengtsson,

Helgesen,

Wang

et al. 2024

Preprint

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“…However, future experiments are to be conducted by culturing and subsequent biochemical tests to confirm the metabolic roles of these vibrios in our samples. In a recent study, the microbiota in the gut ecosystems of red urchin Mesocentrotus franciscanus and the purple urchin Strongylocentrotus purpuratua from Southern California Kelp Forest and barrens of Southern California revealed complex habitat-specific differences [79]. The taxa distribution in these urchins and our study mainly showed insignificant common-ality.…”

Section: Discussionsupporting

confidence: 40%

“…Interestingly, the gut microbiota of red urchin Loxechinus albus from aquaculture environment [80], Antarctic heart urchins (Spatangoida) Abatus agassizii [81], green urchins Lytechinus variegatus from the U.S. Gulf of Mexico [24,25,[82][83][84], and purple urchins Strongylocentrotus purpuratus from the U.S. Oregon Coast [20] showed abundant members of the family Campylobacteraceae. In contrast, Strongylocentrotus purpuratus from Southern California Kelp Forest and barrens had insignificant abundance (<1%) of the Campylobacteraceae [79]. This observation further emphasizes the possibility that diet in the inhabiting ecosystems likely promotes specific taxonomic composition in the urchin gut environment [85].…”

Section: Discussionmentioning

confidence: 88%

“…The taxa distribution in these urchins and our study mainly showed insignificant common-ality. Such habitat-specific diverse taxa distribution in urchins has been implicated in the available diet, temperature, salinity, and other environmental factors [79]. Interestingly, the gut microbiota of red urchin Loxechinus albus from aquaculture environment [80], Antarctic heart urchins (Spatangoida) Abatus agassizii [81], green urchins Lytechinus variegatus from the U.S. Gulf of Mexico [24,25,[82][83][84], and purple urchins Strongylocentrotus purpuratus from the U.S. Oregon Coast [20] showed abundant members of the family Campylobacteraceae.…”

Section: Discussionmentioning

confidence: 99%

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Microbial Composition and Genes for Key Metabolic Attributes in the Gut Digesta of Sea Urchins Lytechinus variegatus and Strongylocentrotus purpuratus Using Shotgun Metagenomics

Hakim

Green

Watts

et al. 2021

CIMB

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This paper describes the microbial community composition and genes for key metabolic genes, particularly the nitrogen fixation of the mucous-enveloped gut digesta of green (Lytechinus variegatus) and purple (Strongylocentrotus purpuratus) sea urchins by using the shotgun metagenomics approach. Both green and purple urchins showed high relative abundances of Gammaproteobacteria at 30% and 60%, respectively. However, Alphaproteobacteria in the green urchins had higher relative abundances (20%) than the purple urchins (2%). At the genus level, Vibrio was dominant in both green (~9%) and purple (~10%) urchins, whereas Psychromonas was prevalent only in purple urchins (~24%). An enrichment of Roseobacter and Ruegeria was found in the green urchins, whereas purple urchins revealed a higher abundance of Shewanella, Photobacterium, and Bacteroides (q-value < 0.01). Analysis of key metabolic genes at the KEGG-Level-2 categories revealed genes for amino acids (~20%), nucleotides (~5%), cofactors and vitamins (~6%), energy (~5%), carbohydrates (~13%) metabolisms, and an abundance of genes for assimilatory nitrogen reduction pathway in both urchins. Overall, the results from this study revealed the differences in the microbial community and genes designated for the metabolic processes in the nutrient-rich sea urchin gut digesta, suggesting their likely importance to the host and their environment.

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“…Sea urchin has been studied for a long time as fisheries resources and model organisms of biology. However, there have been a few studies on general views of their gut microbes' structure, function, and dynamics, particularly using individuallevel metagenome approaches (Hakim et al, 2015, Yao et al, 2019Faddetta et al, 2020;Miller et al, 2021). The abundances of reads assigned to phyla Bacteroidetes and Proteobacteria were observed in the gut of Tripneustes gratilla, and those assigned to phyla Fusobacteria and Proteobacteria in Diadema setosum and Stomopneustes variolaris (Yao et al, 2019), and the order Vibrionales was abundant in wild American green sea urchin (Hakim et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

The Structure and Function of Gut Microbiomes of Two Species of Sea Urchins, Mesocentrotus nudus and Strongylocentrotus intermedius, in Japan

Haditomo

Yonezawa

et al. 2021

Front. Mar. Sci.

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Sea urchin is an indicator of coastal environmental changes in the global warming era, and is also a model organism in developmental biology and evolution. Due to the depletion of wild resources, new aquaculture techniques for improving stocks have been well studied. The gut microbiome shapes various aspects of a host’s physiology. However, these microbiome structures and functions on sea urchins, particularly Mesocentrotus nudus and Strongylocentrotus intermedius which are important marine bioresources commonly found in Japan, have not been fully investigated yet. Using metagenomic approaches including meta16S and shotgun metagenome sequencings, the structures, functions, and dynamics of the gut microbiome of M. nudus and S. intermedius, related to both habitat environment and host growth, were studied. Firstly, a broad meta16S analysis revealed that at the family level, Psychromonadaceae and Flavobacteriaceae reads (38–71%) dominated in these sea urchins, which is a unique feature observed in species in Japan. Flavobacteriaceae reads were more abundant in individuals after rearing in an aquarium with circulating compared to one with running water. Campylobacteraceae and Vibrionaceae abundances increased in both kinds of laboratory-reared sea urchins in both types of experiments. 2-weeks feeding experiments of M. nudus and S. intermedius transplanted from the farm to laboratory revealed that these gut microbial structures were affected by diet rather than rearing environments and host species. Secondly, further meta16S analysis of microbial reads related to M. nudus growth revealed that at least four Amplicon Sequence Variant (ASV) affiliated to Saccharicrinis fermentans, which is known to be a nitrogen (N2) fixing bacterium, showed a significant positive correlation to the body weight and test diameter. Interestingly, gut microbiome comparisons using shotgun metagenome sequencing of individuals showing higher and lower growth rates revealed a significant abundance of “Nitrate and nitrite ammonification” genes in the higher-grown individuals under the circulating water rearing. These findings provide new insights on the structure-function relationship of sea urchin gut microbiomes beyond previously reported nitrogen fixation function in sea urchin in 1950s; we discovered a nitrate reduction function into ammonium for the growth promotion of sea urchin.

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Sea urchin microbiomes vary with habitat and resource availability

Cited by 7 publications

References 36 publications

The sea urchin intestinal microbiome responds dynamically to food intake and contains nitrogen-fixing symbionts

The sea urchin intestinal microbiome responds dynamically to food intake and contains nitrogen-fixing symbionts

Microbial Composition and Genes for Key Metabolic Attributes in the Gut Digesta of Sea Urchins Lytechinus variegatus and Strongylocentrotus purpuratus Using Shotgun Metagenomics

The Structure and Function of Gut Microbiomes of Two Species of Sea Urchins, Mesocentrotus nudus and Strongylocentrotus intermedius, in Japan

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