The Purple Sea Urchin Strongylocentrotus purpuratus Demonstrates a Compartmentalization of Gut Bacterial Microbiota, Predictive Functional Attributes, and Taxonomic Co-Occurrence

Abstract

The sea urchin Strongylocentrotus purpuratus (order Camarodonta, family Strongylocentrotidae) can be found dominating low intertidal pool biomass on the southern coast of Oregon, USA. In this case study, three adult sea urchins were collected from their shared intertidal pool, and the bacteriome of their pharynx, gut tissue, and gut digesta, including their tide pool water and algae, was determined using targeted high-throughput sequencing (HTS) of the 16S rRNA genes and bioinformatics tools. Overall, the gut tissue demonstrated Arcobacter and Sulfurimonas (Epsilonproteobacteria) to be abundant, whereas the gut digesta was dominated by Psychromonas (Gammaproteobacteria), Propionigenium (Fusobacteria), and Flavobacteriales (Bacteroidetes). Alpha and beta diversity analyses indicated low species richness and distinct microbial communities comprising the gut tissue and digesta, while the pharynx tissue had higher richness, more closely resembling the water microbiota. Predicted functional profiles showed Kyoto Encyclopedia of Genes and Genomes (KEGG) Level-2 categories of energy metabolism, membrane transport, cell motility, and signal transduction in the gut tissue, and the gut digesta represented amino acid, carbohydrate, vitamin and cofactor metabolisms, and replication and repair. Co-occurrence network analysis showed the potential relationships and key taxa, such as the highly abundant Arcobacter and Propionigenium, influencing population patterns and taxonomic organization between the gut tissue and digesta. These results demonstrate a trend of microbial community integration, allocation, predicted metabolic roles, and taxonomic co-occurrence patterns in the S. purpuratus gut ecosystem.

Characterization of the Gut Microbiota of the Antarctic Heart Urchin (Spatangoida) Abatus agassizii

“…These results indicate that the conditions within the Abatus host impose successional ecological filters sieving the bacterial diversity of the surrounding sediments and filtering out certain taxa (Stagaman et al, 2017). Analogous differentiation patterns of gut microbiota between gut tissue and digesta have been described in regular sea urchins with a nutrition mode based on a chewing organ (Aristotle's lantern) allowing them to digest algae (Hakim et al, 2016;Hakim et al, 2019), and in corals (Yao et al, 2019). However, given the feeding-mode of Abatus sea urchins and the likeness between their feeding material and their gut content, the detection of distinct bacterial community compositions was unexpected between the external sediment and the gut content samples.…”

“…Shared OTUs were defined as OTUs prevalent in 75% of the samples from the same type in both sites. Co-occurrence analysis was performed on the gut core microbiota of each site through the Co-occurrence Network software (CoNet, v1.1.1) (Faust and Raes, 2016), following the approach described in Hakim et al (2019). Briefly, OTUs with a cumulative sum of relative abundance per sample lower than 100 (i.e., <15% sequence relative abundance) were discarded from the analysis.…”

“…Remarkably, the keystone top candidate of the two Abatus populations was the very same OTU from Desulfobacteraceae (OTU-6 close to the Desulfobacula genus). Taxa belonging to the Desulfobacteraceae family have been previously identified in the literature as potential keystone in other regular (Meziti et al, 2007;Hakim et al, 2016;Hakim et al, 2019) and irregular sea urchin species (Thorsen et al, 2003;Da Silva et al, 2006). The Desulfobacteraceae family members (including Desulfobacula) are sulfate-reducers known to be quantitatively important in the anaerobic degradation of organic matter in coastal marine sediments (Jørgensen, 1982;Bowles et al, 2014).…”

“…The authors demonstrated that the bacteria from the gut of the herbivore sea urchin Strongylocentrotus purpuratus were able to digest the alga Iridophycus flaccidum within a week completely. Since then, there is a growing body of data about the diversity and the composition of the gut microbiota from grazing, wood-feeding and scraping regular echinoids (Becker et al, 2009;Zhang et al, 2014;Hakim et al, 2016;Hakim et al, 2019;Yao et al, 2019). Moreover, the implication of regular sea urchin microbiota has been documented in various aspects of the host life such as its digestion (Sawabe et al, 1995;Thorsen et al, 2003;Lawrence et al, 2013), its immunity (Becker et al, 2009) and the nutrient transfer (Sauchyn and Scheibling, 2009).…”

Differences in Gut Microbial Diversity are Driven by Drug Use and Drug Cessation by Either Compulsory Detention or Methadone Maintenance Treatment

“…All PCR products were sequenced by MiSeq reagent kit version 3 (Illumina, San Diego, CA, USA). Similarly, detailed sequencing methods can be found in the following literature [25,[38][39][40][41][42].…”