Stability of the Microbiome of the Sponge Mycale (Oxymycale) acerata in the Western Antarctic Peninsula

Abstract

The sponge microbiome, especially in Low Microbial Abundance (LMA) species, is expected to be influenced by the local environment; however, contrasting results exist with evidence showing that host specificity is also important, hence suggesting that the microbiome is influenced by host-specific and environmental factors. Despite sponges being important members of Southern Ocean benthic communities, their relationships with the microbial communities they host remain poorly studied. Here, we studied the spatial and temporal patterns of the microbiota associated with the ecologically important LMA sponge M. acerata at sites along ∼400 km of the Western Antarctic Peninsula (WAP) to assess patterns in the core and variable microbial components of the symbiont communities of this sponge species. The analyses of 31 samples revealed that the microbiome of M. acerata is composed of 35 prokaryotic phyla (3 Archaea, 31 Bacteria, and one unaffiliated), being mainly dominated by Proteobacteria with Gammaproteobacteria as the most dominant class. The core community was composed of six prokaryotic OTUs, with gammaproteobacterial OTU (EC94 Family), showing a mean abundance over 65% of the total abundance. Despite some differences in rare OTUs, the core community did not show clear patterns in diversity and abundance associated with specific sites/environmental conditions, confirming a low variability in community structure of this species along the WAP. The analysis at small scale (Doumer Island, Palmer Archipelago) showed no differences in space and time in the microbiome M. acerata collected at sites around the island, sampled in three consecutive years (2016–2018). Our results highlight the existence of a low spatial and temporal variability in the microbiome of M. acerata, supporting previous suggestions based on limited studies on this and other Antarctic sponges.

How does heat stress affect sponge microbiomes? Structure and resilience of microbial communities of marine sponges from different habitats

“…A total of 88 specimens belonging to four demosponge species living in similar shallow rocky benthic environments were collected at three regions representative of polar, temperate, and tropical coastal environments. Mycale acerata (LMA) (Sacristań-Soriano et al, 2020;Happel et al, 2022) and Dendrilla antarctica (LMA) (Koutsouveli et al, 2018;Dıéz-Vives et al, 2020), common yellow sponges in hard bottom benthic environments from polar (Antarctic) waters; and Agelas oroides (HMA) (Vacelet and Donadey, 1977;Blanquer et al, 2013), a lobed orange sponge present in temperate (Mediterranean Sea and Eastern Atlantic) waters; and Acanthella cavernosa (LMA) (Coelho et al, 2018;Cleary et al, 2019), a red spiky sponge present in tropical (Pacific Ocean) waters. Both Antarctic sponges, M. acerata (n=28) and D. antarctica (n=28) were collected at four different stations on Deception and Livingston Islands (South Shetland Islands) (Figure 1 and Table 1).…”

“…This is reflected in "The sponge microbiome project" (Moitinho-Silva et al, 2017a), where the microbiomes of 268 temperate and tropical sponge species were analyzed, but no polar species were included. However, in recent years, the microbiota of 31 Antarctic sponge species (or probably less since some of them were only identified to genus level) have been studied using 16S rRNA amplicon sequencing analysis (Webster et al, 2004;Rodrıǵuez-Marconi et al, 2015;Caŕdenas et al, 2018;Caŕdenas et al, 2019;Lo Giudice et al, 2019;Steinert et al, 2019;Dıéz-Vives et al, 2020;Moreno-Pino et al, 2020;Papale et al, 2020;Sacristań-Soriano et al, 2020;Ruocco et al, 2021;Cristi et al, 2022;Happel et al, 2022). This is still a very small amount, considering that the most recent estimates of sponge species richness in the Southern Ocean and neighboring oceanographic regions were of 400 species as published in the Biogeographic Atlas of the Southern Ocean (Janussen and Downey, 2014).…”

“…There is evidence that these heat waves have caused massive mortality events on marine benthic environments (Garrabou et al, 2009;Hereu and Kersting, 2016;Rubio-Portillo et al, 2016;Hughes et al, 2017;Ereskovsky et al, 2019;Garrabou et al, 2022). Although the sponge microbiome is in general stable across geographical and temporal scales (Erwin et al, 2012;Erwin et al, 2015;Caŕdenas et al, 2019;Happel et al, 2022), it can also be influenced by environmental perturbations (e.g. Webster et al, 2008;Lesser et al, 2016;McDevitt-Irwin et al, 2017).…”

Bacteria Associated with Benthic Invertebrates from Extreme Marine Environments: Promising but Underexplored Sources of Biotechnologically Relevant Molecules

“…Culture-independent methods have been applied to different sponge species to investigate the whole community, collected all around Antarctica, at sites in McMurdo Sound and Terra Nova Bay (Ross Sea, Antarctica), Antarctic Peninsula, South Shetland Islands, and Palmer Archipelago (e.g., [ 135 , 136 , 137 , 138 , 139 , 140 , 141 , 142 , 143 , 144 , 145 , 146 ]). Webster et al [ 135 ] first studied Antarctic-sponge-associated prokaryotic communities.…”

“…Rodríguez-Marconi et al [ 136 ] highlighted that Antarctic-sponge-associated microbial communities differed at the phylum level from those known for temperate and tropical ecosystems. The assessment of host-specificity was the main aim of recent works by Cárdenas et al [ 138 ], Sacristán-Soriano [ 142 ], and Happel et al [ 143 ], who found a high similarity among the microbiota of cold-water sponge species collected from different Antarctic sites. Cristi et al [ 145 ] reported a high degree of specificity of bacterial symbiotic community in Hymeniacidon torquata , suggesting reduced presence of transient bacteria.…”