Chemosynthetic ectosymbiosis reported in the predatory anchialine cave endemic, Xibalbanus tulumensis (Yager, 1987) (Remipedia)

Abstract

Mutualisms between chemosynthetic microbes and invertebrates form the basis of foodwebs in dark, extreme habitats (hydrothermal vents, cold seeps) and have likely facilitated the invasion of extreme underwater caves, as well. Anchialine caves often include distinct water layers of varying concentrations of dissolved oxygen and sulfide and provide an ideal system for the discovery of chemosynthetically based systems and novel symbioses. These caves can be harsh environments for eukaryotes, but they contain gradients favorable for chemosynthetic symbiotic microbes. Here, we provide evidence of chemosynthetic ectosymbiosis in a member of the Remipedia, Xibalbanus tulumensis (Yager, 1987), through electron microscopy and stable isotope analysis. Remipedes are considered to be top predators due to anecdotal observations of feeding in the lab and field, and description of venomous apparati; but they may supplement their diet with microbes. This finding sheds light on opportunistic feeding behaviors that may have evolved to combat resource-limited environments, such as dark, underwater caves.

Community Structure, Abundance and Potential Functions of Bacteria and Archaea in the Sansha Yongle Blue Hole, Xisha, South China Sea

“…Anchialine caves generally support complex and diverse microbial assemblages, but the microbial communities in caves were poorly understand, especially for archaea. Until now, only a few direct studies within caves have been carried out (Holmes et al, 2001; Seymour et al, 2007; Garman et al, 2011; Gonzalez et al, 2011; Humphreys et al, 2012; Pakes, 2013; Busquets et al, 2014; Davis and Garey, 2018). In this study, the other nine caves were chosen to compare the dominant groups and dominant predicted ecological functions in the Yongle Blue Hole (Table 4).…”

“…To date, many anchialine caves have been partially explored, including the Saipan Blue Hole (the Pacific Ocean), the Dahab Blue Hole (Egypt), the Faanu Madugau’s Blue Hole (the Indian Ocean), the Gozo Blue Hole (the Mediterranean Sea) and the Dean’s Blue Hole (the Bahama Islands). The water exchange of anchialine caves with other marine habitats is severely restricted, resulting in the relatively independent environments and special physical-chemical parameters in these caves (Iliffe and Kornicker, 2009; Pakes, 2013; Pérez-Moreno et al, 2016). Little or no photosynthetic oxygen production, stratified water columns and restricted vertical mixing contribute to the anoxic or micro-oxic environment and hydrogen sulfide in anchialine caves (Iliffe, 2000; Seymour et al, 2007; Becking et al, 2011; Gonzalez et al, 2011).…”

Life in the Underworld: Anchialine cave biology in the era of speleogenomics

“…Cave food webs have been regarded as nutrient poor and dependent on external inputs of nutrients such as decaying organic matter (Dickson, 1975;Sket, 1996;Neisch et al, 2012), but recent discoveries have attributed considerable importance to the chemosynthetic activity of bacterial communities Pohlman et al, 1997;Engel et al, 2004;Engel, 2007;Seymour et al, 2007;Gonzalez et al, 2011;Humphreys et al, 2012;Pakes & Mejía-Ortíz, 2014), particularly with increasing distances from cave openings (Neisch et al, 2012). In fact, productivity of cave chemoautotrophic communities appears to correlate with diversity of heterotrophic microbes and of macro-invertebrates in higher trophic levels, which suggests that microbial diversity plays a role in mediating cave biodiversity (Engel, 2007;Porter et al, 2009).…”

“…Chemosynthetic ectosymbioses between bacteria and several invertebrate phyla have been documented in similar ecosystems (Dubilier et al, 2008;Goffredi, 2010), including freshwater caves (Dattagupta et al, 2009;Bauermeister et al, 2012). Recent studies suggest that analogous interactions occur in anchialine systems, with both ecto-and endosymbioses of chemoautotrophic bacteria having been found in two crustacean taxa (the remipede Xibalbanus tulumensis and the atyid shrimp Typhlatya pearsei) from anchialine caves Pakes & Mejía-Ortíz, 2014). Other microbiota also present in anchialine caves include microscopic eukaryotes such as fungi, protozoa, and rotifers, but documentation on their biodiversity and ecological roles in anchialine caves is limited (Engel, 2007).…”

“…Remipede larvae are so far only known from a single species in one cave (Koenemann et al, 2007b;2009b;Olesen et al, 2014). Recent investigations of the remipede Xibalbanus tulumensis (Yager, 1987) have found that in addition to feeding from particulate matter in the water column, this species harbors chemosynthetic bacteria in ectosymbiosis that allow for the uptake of inorganic carbon as a supplement to their diet (Pakes & Mejía-Ortíz, 2014). Furthermore, X. tulumensis has been shown to employ venom to capture and digest atyid shrimp, which makes it the first venomous crustacean ever documented (von Reumont et al, 2014).…”