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

Abstract

Abatus agassizii is an irregular sea urchin species that inhabits shallow waters of South Georgia and South Shetlands Islands. As a deposit-feeder, A. agassizii nutrition relies on the ingestion of the surrounding sediment in which it lives barely burrowed. Despite the low complexity of its feeding habit, it harbors a long and twice-looped digestive tract suggesting that it may host a complex bacterial community. Here, we characterized the gut microbiota of specimens from two A. agassizii populations at the south of the King George Island in the West Antarctic Peninsula. Using a metabarcoding approach targeting the 16S rRNA gene, we characterized the Abatus microbiota composition and putative functional capacity, evaluating its differentiation among the gut content and the gut tissue in comparison with the external sediment. Additionally, we aimed to define a core gut microbiota between A. agassizii populations to identify potential keystone bacterial taxa. Our results show that the diversity and the composition of the microbiota, at both genetic and predicted functional levels, were mostly driven by the sample type, and to a lesser extent by the population location. Specific bacterial taxa, belonging mostly to Planctomycetacia and Spirochaetia, were differently enriched in the gut content and the gut tissue, respectively. Predictive functional profiles revealed higher abundance of specific pathways, as the sulfur cycle in the gut content and the amino acid metabolism, in the gut tissue. Further, the definition of a core microbiota allowed to obtain evidence of specific localization of bacterial taxa and the identification of potential keystone taxa assigned to the Desulfobacula and Spirochaeta genera as potentially host selected. The ecological relevance of these keystone taxa in the host metabolism is discussed.

Schizasterid Heart Urchins Host Microorganisms in a Digestive Symbiosis of Mesozoic Origin

“…Confirming our microscopic results, OTUs most closely related to spirochetes were also very abundant in the ICs of B. townsendi and A. cordatus , but were not recovered in any of the other gut compartments. In contrast, a recent study found spirochetes primarily of the genus Spirochaeta in abundance in the main gut tissue of the schizasterid Abatus agassizii , and identified these taxa as part of its gut microbiome ( Schwob et al, 2020 ). However, this particular species of Abatus does not possess an IC ( Ziegler, 2014 ).…”

“…An increasing number of studies are beginning to shed light on the gut microbiomes found in various echinoderm taxa, among them several deposit-feeding sea cucumber ( Gao et al, 2014 ; Yamazaki et al, 2016 ; Wang et al, 2018 ; Pagán-Jiménez et al, 2019 ; Weigel, 2020 ) and sea urchin species ( Thorsen, 1999 ; Thorsen et al, 2003 ; da Silva et al, 2006 ; Schwob et al, 2020 ). However, most of these analyses focus on microbial organisms found in the main digestive tract, while the present study provides data permitting a comparison between the microbiomes found inside the main gut compartments and a specialized digestive tract derivative.…”

“…As the initial microbial community passes through the gut, the transient microbiome may change due to the interactions of microbes with gut contents or their host as well as the conditions inside the digestive tract. Recently, such a selection process was inferred to occur in the digestive tract of the schizasterid A. agassizii ( Schwob et al, 2020 ). However, in marine deposit feeders that lack hindgut diverticula, most of this modified microbial community is likely washed out once the sediment reaches the anus.…”

“…This is reminiscent of a recently described association between a marine sediment spirochete and a sulfate-reducing Desulfovibrio strain that were studied in co-culture, and where the spirochete produces fermentation products for the sulfate reducer ( Shivani et al, 2016 ). However, in echinoderms active sulfate reduction can lead to toxicity for the host in these types of symbioses ( De Ridder and Foret, 2001 ; De Ridder and Saucède, 2020 ; Schwob et al, 2020 ), but this may be ameliorated by sulfur-oxidizing bacteria observed in the IC that remove sulfide from the organ. Tests of these hypotheses will require a comprehensive functional characterization of the IC’s microbial community.…”

“…These observations could indicate that the schizasterid IC can only be found in species that inhabit a specific zone below the sediment surface where conditions of the surrounding sediment are suitable to support the IC’s digestive symbiosis. In fact, the reduction or even complete absence of the organ in schizasterids such as Pseudabatus, Amphipneustes , or Brachysternaster as well as most species of Abatus ( Ziegler, 2014 ) could be related to a change in lifestyle, as these taxa have been observed to be secondarily semi-infaunal or even entirely epifaunal organisms ( Larrain, 1985 ; Pearse and McClintock, 1990 ; David et al, 2005 ; Thompson and Riddle, 2005 ; Sumida et al, 2008 ; Schwob et al, 2020 ). A test for this hypothesized change in lifestyle would be a comparison of denuded tests of the different schizasterid species, as shape of the anterior ambulacrum correlates with burrowing depth and sediment structure ( Mortensen, 1951 ; Chesher, 1963 ; Kanazawa, 1992 ; Bromley et al, 1995 ).…”