More Than Expected From Old Sponge Samples: A Natural Sampler DNA Metabarcoding Assessment of Marine Fish Diversity in Nha Trang Bay (Vietnam)

Abstract

Sponges have recently been proposed as ideal candidates to act as natural samplers for environmental DNA due to their efficiency in filtering water. However, validation of the usefulness of DNA recovered from sponges to reveal vertebrate biodiversity patterns in Marine Protected Areas is still needed. Additionally, nothing is known about how different sponge species and morphologies influence the capture of environmental DNA and whether biodiversity patterns obtained from sponges are best described by quantitative or qualitative measures. In this study, we amplified and sequenced a vertebrate specific 12S barcode with a set of universal PCR primers (MiFish) for metabarcoding environmental DNA from fishes, to unveil fine-scale patterns of fish communities from natural-sampler DNA retrieved from 64 sponges (16 species) located in eutrophic and well-preserved coral reefs in Nha Trang Bay (central Vietnam). Ninety tropical fish species were identified from the sponges, corresponding to one third of the total local ichthyofauna reported from previous extensive conventional surveys. Significant differentiation in fish communities between eutrophic and well-preserved environments was observed, albeit eutrophication only explained a modest proportion of the variation between fish communities. Differences in efficiency of capturing fish environmental DNA among sponge species or morphologies were not observed. Overall, the majority of detected fish species corresponded to reef-associated small-sized species, as expected in coral reefs environments. Remarkably, pelagic, migratory, and deep-sea fish species were also recovered from sponge tissues, pointing out the ability of sponge natural sampled DNA to detect fishes that were not permanently associated to the biomes where the sponges were sampled. These results highlight the suitability of natural samplers as a cost-effective way to assess vertebrate diversity in hyper-diverse environments.

Assessing the utility of marine filter feeders for environmental DNA (eDNA) biodiversity monitoring

“…Interestingly, sponges might obtain higher spatial resolutions compared to aquatic eDNA in certain instances, as inadvertent water mixing from Niskin sampling resulted in highly abundant eDNA signals from the LSL being observed in aquatic eDNA samples collected at depth, e.g., Anguilla dieffenbachii (New Zealand longfin eel), Galaxias brevipinnis (climbing galaxias fish), Gobiomorphus cotidianus (freshwater common bully), and Trichosurus vulpecula (common brushtail possum). Therefore, our results provide conclusive evidence that sponges naturally accumulate eDNA through either their filter-feeding strategy or the entrapment of particulate matter into the tissue matrix via current flow, or both (Mariani et al, 2019; Turon et al, 2020). Hence, the time-intensive pre-processing step of active filtration, currently limiting sample number and volume (Majaneva et al, 2018; Takasaki et al, 2021), could potentially be omitted by incorporating sponge eDNA into the sampling strategy.…”

“…The power of aquatic eDNA surveys is the ability to retrieve information about a broad range of taxonomic groups, made possible by the complexity of the eDNA signals contained within water (Ruppert et al, 2019). Thus far, vertebrate diversity has been the focus of sponge eDNA research (Mariani et al, 2019; Turon et al, 2020). The majority of extracted DNA, however, will originate from the host.…”

“…Recently, alternative options to active filtration have been explored to circumvent the need for the time-intensive process of vacuum filtration and facilitate the implementation of large-scale eDNA surveys (Bessey et al, 2021; Bowers et al, 2021; Kirtane et al, 2020; Mariani et al, 2019; Turon et al, 2020; Verdier et al, 2021; Yamahara et al, 2019). Passive filtration strategies, whereby filter membranes (Bessey et al, 2021) and other DNA-absorbing matrices (Kirtane et al, 2020) are submerged in the environment, have successfully captured eDNA in seawater.…”

“…These organisms may be especially useful for eDNA surveys, because they can filter large volumes of water - sponges filter up to 900 times their volume of sea water per day (Gökalp et al, 2020), while bivalves can filter over 200 L per day (Berge et al, 2006). While filter feeders are scattered across the tree of life (Hickman et al, 1995), only the eDNA accumulation efficiency of sponges (Mariani et al, 2019; Turon et al, 2020) and shrimp (Siegenthaler et al, 2019) has, thus far, been investigated. Information on other filter-feeding taxa, development of optimal eDNA extraction protocols, and comparative studies determining the comparability between aquatic and filter feeder eDNA are currently lacking.…”

Framing Cutting-Edge Integrative Deep-Sea Biodiversity Monitoring via Environmental DNA and Optoacoustic Augmented Infrastructures

“…For this purpose, eDNA water sampling should also be provided in real-time by autonomous and independent samplers (e.g., Yamahara et al, 2019;Hansen et al, 2020;Jacobsen, 2021;Moore et al, 2021), with prototypes presently under construction (e.g., the Adjustable Volume eDNA Sampler 1 , and the Robotic Cartridge Sampling Instrument-RoCSI 2 ) or that can be adjusted for this purpose, as the SALSA system (Kersten et al, 2019;Brandt et al, 2021) 3 . An alternative to water samplers, would be an opportunistic use of filter feeding organisms such as sponges or bivalves, that act as natural "DNA traps, " concentrating eDNA from water that can be retrieved at different time points (Mariani et al, 2019;Turon et al, 2020;Weber et al, 2021). The advantage of adding eDNA to ecological monitoring protocols is its ability to cross-validate data from other methodologies (e.g., imaging) (e.g., Aguzzi et al, 2019).…”