Symbiosis and microbiome flexibility in calcifying benthic foraminifera of the Great Barrier Reef

Abstract

BackgroundSymbiosis is a phenomenon that allows organisms to colonise a wide range of environments and occupy a variety of ecological niches in marine environments. Large benthic foraminifera (LBF) are crucial marine calcifiers that rely on photo-endosymbionts for growth and calcification, yet the influence of environmental conditions in shaping their interactions with prokaryotic and eukaryotic associates is poorly known.ResultsHere, we used next-generation sequencing to identify eukaryotic photosynthesizing and prokaryotic microbes associated with the common LBF Amphistegina lobifera across a physio-chemical gradient on the Great Barrier Reef (GBR). We collected samples from three reef sites located in the inner-, mid- and outer-shelf regions of the northern section of the GBR. Results showed the consistent presence of Bacillaryophyta as the main eukaryotic taxa associated with A. lobifera across all reef sites analysed; however, the abundance and the diversity of prokaryotic organisms varied among reef sites. Inner-shelf specimens showed the highest diversity of prokaryote associates, with a total of 231 genotypes in their core microbiome. A total of 30 taxa were identified in the core microbiome across all reef sites. Within these taxa, Proteobacteria was the most abundant bacteria present. The presence of groups such as Actinobacteria was significantly correlated with inner-shelf populations, whereas the abundance of Bacteroidetes and Firmicutes was associated with A. lobifera collected from mid- and outer-shelf reef sites.ConclusionsWe found that benthic foraminifera form stable and persistent symbiosis with eukaryotic partners, but flexible and site-specific associations with prokaryotic microbes that likely influence the ecological success of these crucial calcifying organisms on the GBR.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-017-0257-7) contains supplementary material, which is available to authorized users.

Evolutionary significance of the microbial assemblages of large benthic Foraminifera

“…Morphological studies showed that while LBF commonly host a single dominant symbiont species at any given time, several other diatom species can be present at low abundances (Lee et al, ), and some flexibility in these host–symbiont associations is usually observed. However, molecular studies demonstrate that this diversity is likely to have been underestimated by morphological studies (Holzmann, Berney, & Hohenegger, ; Prazeres et al, ). Molecular studies of diatom symbionts in LBF also suggest a strong, species‐specific host–symbiont relationship (Holzmann et al, ; Schmidt et al, , ; Barnes, ; Prazeres et al, ).…”

“…However, molecular studies demonstrate that this diversity is likely to have been underestimated by morphological studies (Holzmann, Berney, & Hohenegger, ; Prazeres et al, ). Molecular studies of diatom symbionts in LBF also suggest a strong, species‐specific host–symbiont relationship (Holzmann et al, ; Schmidt et al, , ; Barnes, ; Prazeres et al, ). Diatom‐bearing species also have associations with other groups of algae such as the green microalga Chlorella (Lee, ), and possibly with rhodophytes, usually at very low relative densities (Prazeres et al, ).…”

“…Molecular studies of diatom symbionts in LBF also suggest a strong, species‐specific host–symbiont relationship (Holzmann et al, ; Schmidt et al, , ; Barnes, ; Prazeres et al, ). Diatom‐bearing species also have associations with other groups of algae such as the green microalga Chlorella (Lee, ), and possibly with rhodophytes, usually at very low relative densities (Prazeres et al, ). However, given their mixotrophic nature, LBF could be utilising these other algal groups as food sources.…”

“…Similarly, Prazeres et al . () used next‐generation sequencing (NGS) to detect a high relative abundance of cyanobacteria associated with Amphistegina lobifera collected from oligotrophic environments, noting that the higher light availability in these environments could give the cyanobacteria a competitive advantage. As in corals, cyanobacteria could play a role in N‐fixation within the host when conditions are optimal (Lesser et al, ).…”

“…Whereas eukaryotic symbiosis has received considerable attention, prokaryotic symbiosis and the role of bacteria in LBF remains largely unexplored (e.g. Webster et al, ; Prazeres et al, ; Prazeres, ). Not only is the diversity of bacterial communities poorly known, but so is the relationship and role that these bacteria may have in LBF ecology, adaptive potential, and evolution.…”