Intracellular bacteria are common and taxonomically diverse in cultured and in hospite algal endosymbionts of coral reefs

Abstract

Corals house a variety of microorganisms which they depend on for their survival, including endosymbiotic dinoflagellates (Symbiodiniaceae) and bacteria. While cnidarian–microorganism interactions are widely studied, Symbiodiniaceae–bacteria interactions are only just beginning to receive attention. Here, we describe the localization and composition of the bacterial communities associated with cultures of 11 Symbiodiniaceae strains from nine species and six genera. Three-dimensional confocal laser scanning and electron microscopy revealed bacteria are present inside the Symbiodiniaceae cells as well as closely associated with their external cell surface. Bacterial pure cultures and 16S rRNA gene metabarcoding from Symbiodiniaceae cultures highlighted distinct and highly diverse bacterial communities occur intracellularly, closely associated with the Symbiodiniaceae outer cell surface and loosely associated (i.e., in the surrounding culture media). The intracellular bacteria are highly conserved across Symbiodiniaceae species, suggesting they may be involved in Symbiodiniaceae physiology. Our findings provide unique new insights into the biology of Symbiodiniaceae.

Surface Topography, Bacterial Carrying Capacity, and the Prospect of Microbiome Manipulation in the Sea Anemone Coral Model Aiptasia

“…For the two anthozoan models, N. vectensis and Aiptasia, there was little difference in terms of ectodermal topography and bacterial colonization between the two organisms, both at the column and tentacle level. However, microalgal symbionts in the family Symbiodiniaceae (LaJeunesse et al, 2018) were shown to putatively contribute to the composition of coral mucus through their exudates (Brown and Bythell, 2005;Nelson et al, 2013), which affect bacterial association (Matthews et al, 2020), and Symbiodiniaceae were also shown to harbor themselves specific bacteria (Maire et al, 2021). As such, Aiptasia is a model system not only for the study of coral-algal symbiosis, but also for the study of bacterial associations and for testing the capacity for microbiome manipulation as further discussed below.…”

“…It is interesting to note that our bacterial capacity was an order of magnitude higher for symbiotic (10 5 bacterial cells/polyp) in comparison to aposymbiotic (10 4 bacterial cells/polyp) anemones. This difference may arise from the additional niche space provided by the symbiosome, which was previously shown to harbor bacteria (Ainsworth et al, 2015), and through association with Symbiodiniaceae, which harbor their own microbial community (Deines et al, 2020;Maire et al, 2021). Visualization and enumeration of cnidarian-associated bacteria is still relatively rare (Neave et al, 2017;Cooke et al, 2019), in part because of the difficulties associated with fluorescent staining techniques in corals (Wada et al, 2016).…”

“…However, both systems lack the ability to engage in symbioses with microalgal symbionts of the family Symbiodiniaceae (LaJeunesse et al, 2018). Therefore, they may not comprise an ideal model for corals, since association with Symbiodiniaceae affects bacterial assemblage (Ainsworth et al, 2015;Röthig et al, 2016a;Lawson et al, 2018;Maire et al, 2021). To this end, the sea anemone Aiptasia is gaining increasing traction as a coral model due to harboring the same or similar Symbiodiniaceae as scleractinian corals, its simplicity of culturing and clonal propagation, and the fact that Aiptasia anemones can be kept indefinitely in symbiotic and aposymbiotic states (i.e., with and without their microalgal partners) (Weis et al, 2008;Voolstra, 2013), allowing to study the mechanistic underpinnings of the cnidarian-dinoflagellate symbiosis in detail (Baumgarten et al, 2015;Biquand et al, 2017;Cziesielski et al, 2018;Rädecker et al, 2018;Gegner et al, 2019;Simona et al, 2019).…”

Microbiome characterization of defensive tissues in the model anemone Exaiptasia diaphana

“…Potential other roles of coral-associated bacteria include carbon, nitrogen and sulfur cycling, and host protection through the production of antimicrobial compounds or competition with opportunistic bacteria [15,20]. Bacteria are found in all microhabitats in a coral polyp, including the mucus [21], skeleton [22], tissue layers [23,24], gastrodermal cavity [25], the mesoglea [26], and even inside the Symbiodiniaceae cells [27]. However, only a handful of studies have compared community structure in the different body parts of the polyp [23,28,29], where a high variability across the different compartments was found.…”

Development of a free radical scavenging bacterial consortium to mitigate oxidative stress in cnidarians

“…Our goal was to identify bacterial strains suitable for use in a microbiome engineering approach to mitigate the effects of thermal stress in E. diaphana . Given the potential role of ROS in the bleaching process and the prevalence of bacteria in and on hosts (Lesser et al ., 2004; Work and Aeby, 2014) and intracellular Symbiodiniaceae (Ainsworth et al ., 2015; Maire et al ., 2021), our focus was to select diverse E . diaphana –sourced bacterial isolates with an extracellular free radical scavenging (FRS) phenotype.…”