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Wooden Stepping Stones: Diversity and Biogeography of Deep-Sea Wood Boring Xylophagaidae

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Wooden Stepping Stones: Diversity and Biogeography of Deep-Sea Wood Boring Xylophagaidae fmars-07-579959 November 20, 2020 Time: 12:28 # 1 ORIGINAL RESEARCH published: 20 November 2020 doi: 10.3389/fmars.2020.579959 Wooden Stepping Stones: Diversity and Biogeography of Deep-Sea Wood Boring Xylophagaidae Edited by: Marcos Rubal, (Mollusca: Bivalvia) in the North-East University of Porto, Portugal Reviewed by: Atlantic Ocean, With the Description Gonzalo Giribet, Harvard University, United States of a New Genus Anna Marie Holmes, National Museum Wales, Chiara Romano1*†‡, Amandine Nunes-Jorge2‡, Nadine Le Bris3†, Greg W. Rouse4†, United Kingdom Daniel Martin1† and Christian Borowski2*† *Correspondence: 1 Centre d’Estudis Avançats de Blanes (CEAB-CSIC), Blanes, Spain, 2 Max Planck Institute for Marine Microbiology, Bremen, Chiara Romano Germany, 3 Sorbonne Université, CNRS, Observatoire Océanologique de Banyuls (LECOB), Banyuls-sur-Mer, France, [email protected] 4 Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA, United States Christian Borowski [email protected] †ORCID: Wood boring bivalves of the family Xylophagaidae inhabit sunken wood on the deep- Chiara Romano sea floor where they play a key role in the degradation of this organic matter in orcid.org/0000-0001-5078-0082 Nadine Le Bris the ocean. The patchiness of wood-fall habitats is impeding targeted sampling and orcid.org/0000-0002-0142-4847 little is therefore known on xylophagaid biology. We investigated for the first time the Greg W. Rouse orcid.org/0000-0001-9036-9263 diversity and biogeography of Xylophagaidae in the NE-Atlantic and the Mediterranean Daniel Martin over a broad geographic range and in various water depths using experimental orcid.org/0000-0001-6350-7384 wood deployments. We combined morphological and molecular analyses for species Christian Borowski orcid.org/0000-0001-7921-3022 discrimination. A phylogenetic reconstruction based on 18S and 28S rRNA and COI ‡These authors have contributed genes revealed non-monophyly of the type genus, Xylophaga Turton(1822), and led equally to this work us to revise the taxonomy and erect the genus Xylonora gen. nov. COI haplotypes of the most abundant species revealed broad Atlanto-Mediterranean genetic connectivity Specialty section: This article was submitted to for Xylophaga dorsalis and Xylonora atlantica new comb., while genetic connectivity Marine Evolutionary Biology, appears limited for Abditoconus brava across the entrance of the Mediterranean. We Biogeography and Species Diversity, a section of the journal provide the first COI barcode data for Xylophagaidae as a solid base for future taxonomic Frontiers in Marine Science work. Wood deployments in a broad geographic range provided a powerful tool for Received: 03 July 2020 research on Xylophagaidae allowing for conclusions on ecological requirements of Accepted: 29 September 2020 xylophagaid species. Published: 20 November 2020 Citation: Keywords: genetic connectivity, wood falls, Mediterranean, deep sea, phylogeography Romano C, Nunes-Jorge A, Le Bris N, Rouse GW, Martin D and Borowski C (2020) Wooden Stepping INTRODUCTION Stones: Diversity and Biogeography of Deep-Sea Wood Boring The Xylophagaidae Purchon(1941) and the sister family Teredinidae Rafinesque(1815) are among Xylophagaidae (Mollusca: Bivalvia) in the North-East Atlantic Ocean, With the most abundant wood-degrading organisms in the marine realm (Turner, 1973; Wolff, 1979; the Description of a New Genus. Distel, 2003; Distel et al., 2011). Both bivalve families have similar habitats, as they both bore Front. Mar. Sci. 7:579959. in wood which they use as a shelter and they are both considered obligate wood feeders with doi: 10.3389/fmars.2020.579959 limited ability for filter feeding (Purchon, 1941; Saraswathy and Nair, 1971). Nevertheless, their Frontiers in Marine Science| www.frontiersin.org 1 November 2020| Volume 7| Article 579959 fmars-07-579959 November 20, 2020 Time: 12:28 # 2 Romano et al. Diversity and Biogeography of North-East Atlantic Xylophagaidae ecological niches do not overlap. Xylophagaidae live in deep xylophagaids keystone for the associated assemblages (Turner, waters where they colonize wood that has sunk to the sea 1973; Culliney and Turner, 1976; Distel, 2003). floor. Teredinidae, known also as shipworms, colonize driftwood Deep-sea wood falls are highly fragmented and ephemeral in surface waters. Shipworms gained a reputation as pests by sulfidic habitats comparable to other chemosynthetic ecosystems damaging boats and submerged wooden structures ever since (e.g., whale falls, hydrothermal vents, hydrocarbon seeps), but humans started to sail, and their life histories and growth rates they sustain even more rapid ecological cycles (Kalenitchenko are therefore well studied (Haderlie and Mellor, 1973; Culliney, et al., 2018b). Organisms living in such patchy habitats often 1975; MacIntosh et al., 2014). Xylophagaidae in contrast, have develop long-distance dispersal strategies to colonize areas been recorded mostly below 150 m depth down to hadal hundreds of kilometers away (Baco et al., 1999; Tyler and environments at 7,000 m depth (Knudsen, 1961; Turner, 2002; Young, 1999; Van Dover et al., 2002; Breusing et al., 2016). Distel, 2003; Voight, 2008) and many aspects of their life Studies on xylophagaids relied for long on occasionally recovered histories remain unknown. naturally sunken wood, mainly as by-catch in trawl and dredge Xylophagaids and teredinids ingest wood chips they create by hauls. Collections of xylophagaids remained largely untargeted boring with their specialized shells and which then accumulate and very little is known on their distribution mechanisms in a special stomach diverticulum, the caecum (Purchon, 1941; and geographical patterns. A few species have been collected Monari, 2009; Distel et al., 2011). Cellulose, hemicellulose repeatedly at different sites, such as Xylophaga dorsalis (Turton, and lignin, the main wood components, are highly refractory 1819) and Xylophaga atlantica Richards, 1942. Both live in wide polysaccharide polymers that do not hydrolyse easily. Biological geographic areas and from littoral to bathyal depths in the degradation uses cellulolytic enzymes that break them down to northern Atlantic Ocean (Purchon, 1941; Culliney and Turner, easily digestible mono- and disaccharides (Klemm et al., 2005). 1976; Santhakumaran, 1980; Voight, 2007). Many other species Many bacteria and fungi synthesize cellulolytic enzymes, while are only known from single records (Knudsen, 1961; Harvey, most animals do not. Teredinids harbor cellulose-degrading 1996; Turner, 2002; Voight, 2007, 2008), while some occur bacteria in their gills (Waterbury et al., 1983; Distel et al., in abyssal plains or even in deep-sea trenches, thousands of 2002; Distel, 2003) and this symbiosis is considered as the kilometers away from the nearest land mass, where sunken basis for their wood digestion capacity (O’Connor et al., wood is considered extremely rare (Knudsen, 1961; Voight, 2008; 2014). However, an additional combination of cellulolytic Voight and Segonzac, 2012). enzymes produced by the molluscs themselves has been recently Xylophagaidae currently includes six genera: Xylophaga discovered in the caecum (Sabbadin et al., 2018). Xylophagaidae Turton, 1822, Xylopholas Turner, 1972, Xyloredo Turner, 1972, also host endosymbiotic bacteria in the gills (Distel and Feaya Voight, 2019, Abditoconus Voight, 2019, and Spiniapex Roberts, 1997; Bessette et al., 2014; Fagervold et al., 2014; Voight, 2019 (Voight et al., 2019). Xylophaga is the most speciose, Voight, 2015), but their role and metabolic pathways remain containing currently more than 50 species. Historically, the even less studied. vast majority of taxonomic works on Xylophagaidae have based Wood reaches the open ocean by river transport after on morphology, while only two studies also used molecular storm and flood events (Stockton and DeLaca, 1982; West markers; hence little is currently known about their genetic et al., 2011), and after drifting and becoming saturated with diversity (Romano et al., 2014; Voight et al., 2019). The main water it eventually sinks down to the seafloor (Wolff, 1979). diagnostic morphological characters refer to valves, mesoplax, Sunken wood represents high local carbon inputs to the deep siphons, and muscle inserts on inner surfaces of the valves (Tyler sea which generally lacks primary production and receives et al., 2007). These characters and the overall shape of the shells extremely limited phototrophic contributions from the surface may vary among populations and are affected by environmental (Stockton and DeLaca, 1982; Smith et al., 2008). Wood-falls conditions such as wood hardness. Even individuals within the create discrete organic islands on the deep-sea floor harboring same population inhabiting neighboring logs of different wood distinct and specialized fauna mining the wood, breaking it up such as soft pine or hard oak may vary (Turner, 2002). In and thereby supporting wood polymer degradation by cellulolytic addition, extraction of the xylophagaids from wood substrates microorganisms (Kalenitchenko et al., 2018b). Consumption of can be challenging and often lead to fragmentation of specimens oxygen during this process eventually leads to anoxic and sulfidic and damage of their delicate shells. As a result, several species environments providing habitats for chemosynthetic microbial descriptions are based on single or incomplete specimens, lacking communities and invertebrates associated with sulfur-oxidizing information
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