Phylogenetically and Spatially Close Marine Sponges Harbour Divergent Bacterial Communities

Abstract

Recent studies have unravelled the diversity of sponge-associated bacteria that may play essential roles in sponge health and metabolism. Nevertheless, our understanding of this microbiota remains limited to a few host species found in restricted geographical localities, and the extent to which the sponge host determines the composition of its own microbiome remains a matter of debate. We address bacterial abundance and diversity of two temperate marine sponges belonging to the Irciniidae family - Sarcotragus spinosulus and Ircinia variabilis – in the Northeast Atlantic. Epifluorescence microscopy revealed that S. spinosulus hosted significantly more prokaryotic cells than I. variabilis and that prokaryotic abundance in both species was about 4 orders of magnitude higher than in seawater. Polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE) profiles of S. spinosulus and I. variabilis differed markedly from each other – with higher number of ribotypes observed in S. spinosulus – and from those of seawater. Four PCR-DGGE bands, two specific to S. spinosulus, one specific to I. variabilis, and one present in both sponge species, affiliated with an uncultured sponge-specific phylogenetic cluster in the order Acidimicrobiales (Actinobacteria). Two PCR-DGGE bands present exclusively in S. spinosulus fingerprints affiliated with one sponge-specific phylogenetic cluster in the phylum Chloroflexi and with sponge-derived sequences in the order Chromatiales (Gammaproteobacteria), respectively. One Alphaproteobacteria band specific to S. spinosulus was placed in an uncultured sponge-specific phylogenetic cluster with a close relationship to the genus Rhodovulum. Our results confirm the hypothesized host-specific composition of bacterial communities between phylogenetically and spatially close sponge species in the Irciniidae family, with S. spinosulus displaying higher bacterial community diversity and distinctiveness than I. variabilis. These findings suggest a pivotal host-driven effect on the shape of the marine sponge microbiome, bearing implications to our current understanding of the distribution of microbial genetic resources in the marine realm.

Host rules: spatial stability of bacterial communities associated with marine sponges (Irciniaspp.) in the Western Mediterranean Sea

“…The bacterial communities associated with the co‐occurring Mediterranean sponges I. fasciculata , I. variabilis and I. oros were structured primarily by host species and remained largely stable across geographic distances of up to 800 km. These results reinforced the key role of host sponge species on the composition of their symbiotic bacterial communities (Montalvo & Hill, ; Erwin et al ., ; Hardoim et al ., ) and were consistent with high spatial stability reported in previous studies (Taylor et al ., ; Wichels et al ., ; Thiel et al ., ; Schöttner et al ., ), including other Ircinia species (Pita et al ., ). In addition, we revealed overall similar patterns of spatial stability and host specificity between rare and abundant bacteria, as has been found for free‐living microbial communities (Galand et al ., ).…”

Molecular richness and biotechnological potential of bacteria cultured from Irciniidae sponges in the north-east Atlantic

“…Equivalent genotypic richness and diversity measures were observed for both species, despite the trend for slightly higher values in S. spinosulus . Previous results using a cultivation‐independent technique (PCR‐DGGE) supported the picture of moderately higher bacterial richness and diversity in S. spinosulus than in I. variabilis (Hardoim et al ., ). Other cultivation‐dependent studies documented similar genus‐level composition for sponge species from different locations under varied culture conditions, particularly regarding the dominance of Alphaproteobacteria such as Pseudovibrio and Ruegeria (Webster & Hill, ; Thiel & Imhoff, ; Lafi et al ., ; Muscholl‐Silberhorn et al ., ; Sipkema et al ., ).…”

“…Each bag was kept refrigerated inside a cooling container and brought to the laboratory, where sponges were processed immediately. A fragment of each sponge specimen was excised and preserved in 90% ethanol for classical and molecular taxonomic identification, revealing that nine specimens belonged to S. spinosulus and four to I. variabilis (see Hardoim et al ., for procedures). These vouchers were deposited in the Biology Department's zoological collection of the University of the Azores (DBUA.Por).…”

Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix

“…However, recent studies have observed a strong and persistent effect of host species irrespective of geography, microbial abundance, or microbial community complexity. Several studies that have observed a relationship between microbial community structure and environmental variability have also noted strong host effects (e.g., Cleary et al, ; Griffiths et al, ; Hardoim et al, ; Marino et al, ; Reveillaud et al, ), with most of the environmental variability being observed within species. A recent study on geographic variation in the microbiome of the sponge Ircinia campana observed significant variation in microbial communities only over large geographic gradients, but also noted the presence of location‐specific microbial taxa (Marino et al, ).…”