16S rRNA Gene Metabarcoding Indicates Species-Characteristic Microbiomes in Deep-Sea Benthic Foraminifera

Foraminifera are unicellular eukaryotes that are an integral part of benthic fauna in many marine ecosystems, including the deep sea, with direct impacts on benthic biogeochemical cycles. In these systems, different foraminiferal species are known to have a distinct vertical distribution, i.e., microhabitat preference, which is tightly linked to the physico-chemical zonation of the sediment. Hence, foraminifera are well-adapted to thrive in various conditions, even under anoxia. However, despite the ecological and biogeochemical significance of foraminifera, their ecology remains poorly understood. This is especially true in terms of the composition and diversity of their microbiome, although foraminifera are known to harbor diverse endobionts, which may have a significant meaning to each species’ survival strategy. In this study, we used 16S rRNA gene metabarcoding to investigate the microbiomes of five different deep-sea benthic foraminiferal species representing differing microhabitat preferences. The microbiomes of these species were compared intra- and inter-specifically, as well as with the surrounding sediment bacterial community. Our analysis indicated that each species was characterized with a distinct, statistically different microbiome that also differed from the surrounding sediment community in terms of diversity and dominant bacterial groups. We were also able to distinguish specific bacterial groups that seemed to be strongly associated with particular foraminiferal species, such as the family Marinilabiliaceae for Chilostomella ovoidea and the family Hyphomicrobiaceae for Bulimina subornata and Bulimina striata. The presence of bacterial groups that are tightly associated to a certain foraminiferal species implies that there may exist unique, potentially symbiotic relationships between foraminifera and bacteria that have been previously overlooked. Furthermore, the foraminifera contained chloroplast reads originating from different sources, likely reflecting trophic preferences and ecological characteristics of the different species. This study demonstrates the potential of 16S rRNA gene metabarcoding in resolving the microbiome composition and diversity of eukaryotic unicellular organisms, providing unique in situ insights into enigmatic deep-sea ecosystems.