Shipworm Research Articles

Biodegradation of wood exposed in the marine environment: Evaluation of the hazard posed by marine wood-borers in fifteen European sites

The activity of marine wood-borers causes great destruction in maritime wooden structures. Therefore, the aim of this study was to evaluate the hazard posed by marine wood-borers in fifteen European sites, to assist authorities and researchers concerned with the protection of wood in the sea. In northern Europe, Teredo navalis is the species that poses the highest borer hazard while in the Atlantic coast of southern Europe Lyrodus pedicellatus is the most destructive species, with the exception of two sites in Portugal. In these sites, Limnoria tripunctata was more destructive than L. pedicellatus. In the Mediterranean both T. navalis and L. pedicellatus pose a very high borer hazard to wooden structures.Salinity and temperature emerged as the environmental conditions that best explain the occurrence and abundance of wood boring species in the sites surveyed. Three of the species highlighted in this study are warm water species. Therefore their activity might increase in the future, due to global warming. Considering that wood is still a very valuable material for construction, its use for maritime construction should be favoured. Thus research to improve the durability of wooden materials in the marine environment is of paramount importance.

Pelagic larvae of bivalve mollusks of Amursky Bay, Sea of Japan

Larvae of 63 Bivalvia taxa were found in Amursky Bay. Of these, 47 were identified to the species level. Larvae of 55 taxa were found throughout the bay. The highest species diversity was recorded in the northeastern part and in the center of the southern part of the bay, as well as at the exit from it. Larvae of Mactra chinensis, Mytilus coruscus, Crassostrea gigas, Teredo navalis, Mya japonica, and Mysella ventricosa were widely distributed in the bay. The maximum numbers of species were observed in July and September. A comparison of species lists using the set-theory method showed that the species complexes typical of different parts of Amursky Bay are formed under the influence of the Razdolnaya River runoff flow from the north and marine waters coming from the south. The mean density of larvae during the observation period was 1100 specimens/m3 in the northern and 735 specimens/m3 in the southern part of the bay. The highest density of larvae in Amursky Bay was observed at the end of June, the beginning of July, and in September; the minimal larval density occurred in April, May, and August. While the species diversity was similarly high, the density of larvae was significantly higher in Amursky Bay than in the nearby Ussuriisky Bay.

First records of the warm water shipworm Teredo bartschi Clapp, 1923 (Bivalvia, Teredinidae) in Mersin, southern Turkey and in Olhão, Portugal

Bivalves of the family Teredinidae are among the most destructive wood-boring species in the sea. We report the first occurrences of the warm-water shipworm Teredo bartschi in Mersin, Turkey, and Olhao, Portugal. The colonisation of the site in Mersin is likely to have occurred by rafting adults originating from the Red Sea, which passed through the Suez Canal (lessepsian migrants). T. bartschi might have been introduced in Olhao Harbour, Portugal, either by rafting adults with larvae transported by currents or by larvae transported by ships in ballast water. These seem to be the first published records of established T. bartschi populations in the Mediterranean and in northeast Atlantic.

Genetic differentiation among isolates of Teredinibacter turnerae, a widely occurring intracellular endosymbiont of shipworms.

Teredinibacter turnerae is a cultivable intracellular endosymbiont of xylotrophic (woodfeeding)bivalves of the Family Teredinidae (shipworms). Although T. turnerae has been isolated from many shipworm taxa collected in many locations, no systematic effort has been made to explore genetic diversity within this symbiont species across the taxonomic and geographical range of its hosts. The mode of symbiont transmission is unknown. Here, we examine sequence diversity in fragments of six genes (16S rRNA, gyrB, sseA, recA, rpoB and celAB) among 25 isolates of T. turnerae cultured from 13 shipworm species collected in 15 locations in the Atlantic, Pacific and Indian Oceans. While 16S rRNA sequences are nearly invariant between all examined isolates (maximum pairwise difference <0.26%), variation between examined protein-coding loci is greater (mean pairwise difference 2.2–5.9%). Phylogenetic analyses based on each protein-coding locus differentiate the 25 isolates into two distinct and well-supported clades. With five exceptions, clade assignments for each isolate were supported by analysis of alleles of each of the five protein-coding loci. These exceptions include (i) putative recombinant alleles of the celAB and gyrB loci in two isolates (PMS-535T.S.1b.3 and T8510), suggesting homologous recombination between members of the two clades; and (ii) evidence for a putative lateral gene transfer event affecting a second locus (recA) in three isolates (T8412, T8503 and T8513). These results demonstrate that T. turnerae isolates do not represent a homogeneous global population. Instead, they indicate the emergence of two lineages that, although distinct, likely experience some level of genetic exchange with each other and with other bacterial species.

Diversity, environmental requirements, and biogeography of bivalve wood-borers (Teredinidae) in European coastal waters.

BackgroundBivalve teredinids inflict great destruction to wooden maritime structures. Yet no comprehensive study was ever carried out on these organisms in European coastal waters. Thus, the aims of this study were to: investigate the diversity of teredinids in European coastal waters; map their past and recent distributions to detect range expansion or contraction; determine salinity-temperature (S-T) requirements of species; flag, for future monitoring, the species that pose the greatest hazard for wooden structures.ResultsA total of nine teredinid species were found established in European coastal waters. Seven were considered cryptogenic, of unknown origin, and two were considered alien species. Teredo navalis and Nototeredo norvagica were the species with the widest distribution in European waters. Recently, T. navalis has been reported occurring further east in the Baltic Sea but it was not found at a number of sites on the Atlantic coast of southern Europe. The Atlantic lineage of Lyrodus pedicellatus was the dominant teredinid in the southern Atlantic coast of Europe. In the Mediterranean six teredinid species occurred in sympatry, whereas only three of these occurred in the Black Sea. The species that pose the greatest hazard to wooden maritime structures in European coastal areas are T. navalis and the two lineages of L. pedicellatus.ConclusionsCombined data from field surveys and from the literature made it possible to determine the diversity of established teredinid species and their past and recent distribution in Europe. The environmental requirements of species, determined using climatic envelopes, produced valuable information that assisted on the explanation of species distribution. In addition, the observed trends of species range extension or contraction in Teredo navalis and in the two lineages of Lyrodus pedicellatus seem to emphasise the importance of temperature and salinity as determinants of the distribution of teredinids, whereas their life history strategy seems to play an important role on competition.Teredo navalis and pedicellatus-like Lyrodus species should be monitored due to their destructive capability. The two alien species may expand further their distribution range in Europe, becoming invasive, and should also be monitored.

フナクイムシ由来のセルロース分解菌の探索

フナクイムシ由来のセルロース分解菌の探索

Growth, nitrogen fixation, respiration, and a nitrogen budget for cultures of a cosmopolitan diazotrophic endosymbiont (Teredinibacter turnerae) of shipworms

Wood-boring bivalves (Bivalvia, family Teredinidae), also known as shipworms, host dinitrogen-fixing and cellulolytic symbiotic bacteria in gill bacteriocytes, which may be a necessary adaptation to a wooden diet. Although oxygen (O2) inhibits nitrogenase in other species, symbionts are able to fix nitrogen (N) within the gill tissue and provide newly fixed N to the host shipworm. The recent direct evidence of new N incorporation into the host tissue indicates that there are potentially complex nutrient cycles in this symbiosis and uninvestigated controls upon these cycles.To elucidate the mechanisms of this unique N2-fixing symbiosis and determine whether symbionts can excrete newly fixed N, we measured rates of growth, N2-fixation, respiration, and inorganic N content for the cultivated symbiontTeredinibacter turnerae(γ-proteobacteria, strain T7901) under a range of headspace O2conditions. In all conditions, headspace O2did not affect maximum specific N2-fixation and respiration activity, but did influence the rate and timing of growth. These results are consistent with the development of microaerobic conditions through an oxygen gradient in the culture medium, which facilitates N2-fixation and growth. The medium accumulated a small amount of NH4+, which represented 0.5–2.5% of the total N fixed by the culture. We constructed a simple N budget forT. turneraeto assess the role of the major known N sources and sinks. The N budget was not closed, indicating that new N is allocated to currently unidentified sinks, which may include excreted dissolved organic nitrogen.

Pelagic larvae of the bivalves of Ussuriysky Bay, Sea of Japan

Based on materials of plankton surveying carried out in May–October 2008, the species composition, distribution, and density of pelagic larvae of bivalves of the Ussuriysky Bay (Peter the Great Bay, Sea of Japan) were studied. Larvae of 66 taxa were revealed and identified. The Bivalvia larvae occurred in the plankton during the entire period of study. Two areas, the inner and open part of the bay, which vary in the composition, concentration, and terms of larva occurrence in the plankton were distinguished. The larvae of Mytilus coruscus, Mactra chinensis, Modiolus kurilensis, Ruditapes philippinarum, Mya uzenensis and Teredo navalis were the most numerous and widespread. It was shown that despite high taxonomic diversity, the density of Bivalvia larvae in the Ussuriysky Bay was an order of magnitude lower, even in terms of their maximum number, than in other studied areas of the Peter the Great Bay.

Turnerbactin, a novel triscatecholate siderophore from the shipworm endosymbiont Teredinibacter turnerae T7901.

Shipworms are marine bivalve mollusks (Family Teredinidae) that use wood for shelter and food. They harbor a group of closely related, yet phylogenetically distinct, bacterial endosymbionts in bacteriocytes located in the gills. This endosymbiotic community is believed to support the host's nutrition in multiple ways, through the production of cellulolytic enzymes and the fixation of nitrogen. The genome of the shipworm endosymbiont Teredinibacter turnerae T7901 was recently sequenced and in addition to the potential for cellulolytic enzymes and diazotrophy, the genome also revealed a rich potential for secondary metabolites. With nine distinct biosynthetic gene clusters, nearly 7% of the genome is dedicated to secondary metabolites. Bioinformatic analyses predict that one of the gene clusters is responsible for the production of a catecholate siderophore. Here we describe this gene cluster in detail and present the siderophore product from this cluster. Genes similar to the entCEBA genes of enterobactin biosynthesis involved in the production and activation of dihydroxybenzoic acid (DHB) are present in this cluster, as well as a two-module non-ribosomal peptide synthetase (NRPS). A novel triscatecholate siderophore, turnerbactin, was isolated from the supernatant of iron-limited T. turnerae T7901 cultures. Turnerbactin is a trimer of N-(2,3-DHB)-L-Orn-L-Ser with the three monomeric units linked by Ser ester linkages. A monomer, dimer, dehydrated dimer, and dehydrated trimer of 2,3-DHB-L-Orn-L-Ser were also found in the supernatant. A link between the gene cluster and siderophore product was made by constructing a NRPS mutant, TtAH03. Siderophores could not be detected in cultures of TtAH03 by HPLC analysis and Fe-binding activity of culture supernatant was significantly reduced. Regulation of the pathway by iron is supported by identification of putative Fur box sequences and observation of increased Fe-binding activity under iron restriction. Evidence of a turnerbactin fragment was found in shipworm extracts, suggesting the production of turnerbactin in the symbiosis.

The survival of Teredo navalis L. in timber wrapped in TERRAM4000 and a plastic membrane

Since in situ preservation of archaeological material has become more widespread (European Union, 1992) the need to stop an active attack of Teredo navalis, a wood-boring mollusc, on waterlogged archaeological wood has become more urgent. The aim of current study is to examine the ability of two plastic materials (TERRAM4000 and a plastic membrane) to stop both initial attack by T. navalis and their effects on wood with active woodborer degradation. Blocks of pinewood were submerged in the southern part of the Kattegat in Denmark, where shipworm is known to be prolific. After settling and attack had been confirmed, the blocks were removed and wrapped in either TERRAM4000 (polypropylene and polyethylene) or a proprietary plastic membrane (polyethylene), normally used on fishing piles or piers, as a protection against shipworm in Denmark. An optical oxygen sensor was packed together with each block to measure the amount of available oxygen around the wood. After one week the oxygen level around the test blocks wrapped in the plastic membrane had dropped drastically and lead to the death of all shipworms within the test blocks after one-four weeks. Although no new shipworm attacked the wood wrapped in TERRAM4000, the geotextile did not impede the passage of oxygenated seawater, as living individuals were found in the blocks after 46 weeks of wrapping and submersion.

What is the main food source of the shipworm (Teredo navalis)? A stable isotope approach

Stable isotope analysis of soft bodies of the shipworm Teredo navalis demonstrated that this species is mainly feeding on seston by filter feeding in contrast to wood consumption. T. navalis showed similar stable isotope values (δ13C, δ15N) as Mytilus edulis and Crassostrea gigas, which species were attached to the wood instead of boring into.

Boronated tartrolon antibiotic produced by symbiotic cellulose-degrading bacteria in shipworm gills

Shipworms are marine wood-boring bivalve mollusks (family Teredinidae) that harbor a community of closely related Gammaproteobacteria as intracellular endosymbionts in their gills. These symbionts have been proposed to assist the shipworm host in cellulose digestion and have been shown to play a role in nitrogen fixation. The genome of one strain of Teredinibacter turnerae, the first shipworm symbiont to be cultivated, was sequenced, revealing potential as a rich source of polyketides and nonribosomal peptides. Bioassay-guided fractionation led to the isolation and identification of two macrodioloide polyketides belonging to the tartrolon class. Both compounds were found to possess antibacterial properties, and the major compound was found to inhibit other shipworm symbiont strains and various pathogenic bacteria. The gene cluster responsible for the synthesis of these compounds was identified and characterized, and the ketosynthase domains were analyzed phylogenetically. Reverse-transcription PCR in addition to liquid chromatography and high-resolution mass spectrometry and tandem mass spectrometry revealed the transcription of these genes and the presence of the compounds in the shipworm, suggesting that the gene cluster is expressed in vivo and that the compounds may fulfill a specific function for the shipworm host. This study reports tartrolon polyketides from a shipworm symbiont and unveils the biosynthetic gene cluster of a member of this class of compounds, which might reveal the mechanism by which these bioactive metabolites are biosynthesized.

Strategies for Protection of Wooden Underwater Cultural Heritage in the Baltic Sea Against Marine Borers. The EU Project ‘WreckProtect’

Marine borers constitute a great danger to historical shipwreck in marine environments as they are able to decompose wood material in just a few years. Recently, there have been indications that the marine borer Teredo navalis is spreading into the brackish Baltic sea, where thousands of invaluable historical wrecks for centuries have had unique preservation conditions. The WreckProtect project was a coordination and support action funded by the European Commission within the 7th Framework Program. The main objective of the project was to develop tools for predicting the spread of marine borers into the Baltic and to evaluate methods for in situ protection of the historical wreck and submerged settlements. This paper gives a summary final report of the project and an overview of results.

Microbial Distribution and Abundance in the Digestive System of Five Shipworm Species (Bivalvia: Teredinidae)

Marine bivalves of the family Teredinidae (shipworms) are voracious consumers of wood in marine environments. In several shipworm species, dense communities of intracellular bacterial endosymbionts have been observed within specialized cells (bacteriocytes) of the gills (ctenidia). These bacteria are proposed to contribute to digestion of wood by the host. While the microbes of shipworm gills have been studied extensively in several species, the abundance and distribution of microbes in the digestive system have not been adequately addressed. Here we use Fluorescence In-Situ Hybridization (FISH) and laser scanning confocal microscopy with 16S rRNA directed oligonucleotide probes targeting all domains, domains Bacteria and Archaea, and other taxonomic groups to examine the digestive microbiota of 17 specimens from 5 shipworm species (Bankia setacea, Lyrodus pedicellatus, Lyrodus massa, Lyrodus sp. and Teredo aff. triangularis). These data reveal that the caecum, a large sac-like appendage of the stomach that typically contains large quantities of wood particles and is considered the primary site of wood digestion, harbors only very sparse microbial populations. However, a significant number of bacterial cells were observed in fecal pellets within the intestines. These results suggest that due to low abundance, bacteria in the caecum may contribute little to lignocellulose degradation. In contrast, the comparatively high population density of bacteria in the intestine suggests a possible role for intestinal bacteria in the degradation of lignocellulose.

Evaluation of wooden materials deteriorated by marine-wood boring organisms in the Black Sea

Marine borers can destroy wooden structures exposed to the marine environment and cause great monetary loss. In the region of Amasra of the Black Sea in Turkey, ships continue to be built from wood, mainly Castanea sativa (sweet chestnut) and Quercus petraea (sessile oak) and therefore are subject to destruction by marine borers. Copper-chromium-arsenic (CCA), used to be one of the most common wood preservatives used in Turkey. However, in this area its ecacy against mari- ne borers is unknown. � e resistance of untreated and CCA-treated samples of chestnut, oak and Scots pine (Pinus sylvestris) was examined and aer twelve months evaluated in two ways, EN 275, and a non-destructive measurement for dynamic modulus of elasticity (MOE). Untreated samples, particularly Scots pine were severely attacked by Teredo navalis. Treated samples of oak and chestnut were moderately attacked while treated samples of Scots pine sapwood and heartwood were sound. Severity of wood boring attack determined using MOE showed a very good correlation with that de- termined by visual assessment in untreated wood, and a good correlation for treated wood. Dynamic MOE allows rapid on-site evaluation rather than measurements within a laboratory and also without causing damage to the structures being evaluated.

Studies on the Cellulose-Degrading System in a Shipworm and its Potential Applications

The great shipworm Teredo navalis is a bivalve of the Teredinidae family known for its efficient ability at degrading wood and feeding on sugar molecules constituting its building blocks. The aim of this study was to identify new endogenous genes encoding cellulose-degrading enzymes from the shipworm. We suspect those genes to play an important role in the efficient biomass degradation of T. navalis. We constructed an expressed sequence tag (EST) database of 3‘end cDNAs prepared by reverse transcription of mRNAs prepared from the shipworm whole body. A GS FLX 454 pyrosequencing system was used to sequence the transcriptome. A total of 12,879 contigs and 80,891 singlets were obtained and probed using blast2go. In this short paper we present the preliminary findings of our study.

Metagenomic cellulases highly tolerant towards the presence of ionic liquids—linking thermostability and halotolerance

Cellulose is an important renewable resource for the production of bioethanol and other valuable compounds. Several ionic liquids (ILs) have been described to dissolve water-insoluble cellulose and/or wood. Therefore, ILs would provide a suitable reaction medium for the enzymatic hydrolysis of cellulose if cellulases were active and stable in the presence of high IL concentrations. For the discovery of novel bacterial enzymes with elevated stability in ILs, metagenomic libraries from three different hydrolytic communities (i.e. an enrichment culture inoculated with an extract of the shipworm Teredo navalis, a biogas plant sample and elephant faeces) were constructed and screened. Altogether, 14 cellulolytic clones were identified and subsequently assayed in the presence of six different ILs. The most promising enzymes, CelA2, CelA3 (both derived from the biogas plant) and CelA84 (derived from elephant faeces), showed high activities (up to 6.4 U/mg) in the presence of 30% (v/v) ILs. As these enzymes were moderately thermophilic and halotolerant, they retained 40% to 80% relative activity after 34 days in 4 M NaCl, and they were benchmarked with two thermostable enzymes, CelA from Thermotoga maritima and Cel5K from a metagenome library derived from Avachinsky crater in Kamchatka. These enzymes also exhibited high activity (up to 11.1 U/mg) in aqueous IL solutions (30% (v/v)). Some of the enzymes furthermore exhibited remarkable stability in 60% (v/v) IL. After 4 days, CelA3 and Cel5K retained up to 79% and 100% of their activity, respectively. Altogether, the obtained data suggest that IL tolerance appears to correlate with thermophilicity and halotolerance.

Molecular phylogeny of Pholadoidea Lamarck, 1809 supports a single origin for xylotrophy (wood feeding) and xylotrophic bacterial endosymbiosis in Bivalvia

The ability to consume wood as food (xylotrophy) is unusual among animals. In terrestrial environments, termites and other xylotrophic insects are the principle wood consumers while in marine environments wood-boring bivalves fulfill this role. However, the evolutionary origin of wood feeding in bivalves has remained largely unexplored. Here we provide data indicating that xylotrophy has arisen just once in Bivalvia in a single wood-feeding bivalve lineage that subsequently diversified into distinct shallow- and deep-water branches, both of which have been broadly successful in colonizing the world’s oceans. These data also suggest that the appearance of this remarkable life habit was approximately coincident with the acquisition of bacterial endosymbionts. Here we generate a robust phylogeny for xylotrophic bivalves and related species based on sequences of small and large subunit nuclear rRNA genes. We then trace the distribution among the modern taxa of morphological characters and character states associated with xylotrophy and xylotrepesis (wood-boring) and use a parsimony-based method to infer their ancestral states. Based on these ancestral state reconstructions we propose a set of plausible hypotheses describing the evolution of symbiotic xylotrophy in Bivalvia. Within this context, we reinterpret one of the most remarkable progressions in bivalve evolution, the transformation of the “typical” myoid body plan to create a unique lineage of worm-like, tube-forming, wood-feeding clams. The well-supported phylogeny presented here is inconsistent with most taxonomic treatments for xylotrophic bivalves, indicating that the bivalve family Pholadidae and the subfamilies Teredininae and Bankiinae of the family Teredinidae are non-monophyletic, and that the principle traits used for their taxonomic diagnosis are phylogenetically misleading.

New threats of an old enemy: The distribution of the shipworm Teredo navalis L. (Bivalvia: Teredinidae) related to climate change in the Port of Rotterdam area, the Netherlands

The effects of four climate change scenarios for the Netherlands on the distribution of the shipworm upstream of the Rhine–Meuse estuary are described. Global warming will cause dry and warmer summers and decreased river discharges. This will extend the salinity gradient upstream in summer and fall and may lead to attacks on wooden structures by the shipworm. Scenarios including one or two degree temperature increases by 2050 compared to 1990 with a weak change in the air circulation over Europe will lead to an increased chance of shipworm damage upstream from once in 36years to once in 27 or 22years, respectively; however, under a strong change in air circulation, the chance of shipworm damage increases to once in 6 or 3years, respectively. The upstream expansion of the distribution of the shipworm will also be manifested in other northwest European estuaries and will be even stronger in southern Europe.

Distribution, settlement, and growth of first-year individuals of the shipworm Teredo navalis L. (Bivalvia: Teredinidae) in the Port of Rotterdam area, the Netherlands

During the period 2004–2008 the distribution, settlement, and growth of first-year shipworms ( Teredo navalis L., 1758) was studied by exposing fir and oak panels in the Port of Rotterdam area, which is situated in the Rhine-Meuse estuary in the Netherlands and covers the complete salinity gradient. Shipworms were found yearly in the western large polyhaline harbours. On only a few occasions were they were found in harbours that showed large seasonal and daily fluctuations in salinity. In 2006 the shipworm was found in fir panels 20 km upstream from the polyhaline harbours, demonstrating their ability to travel with the tidal currents over considerable distances and to settle once the abiotic conditions become favourable. Although the water temperatures allowed them to breed from April until November, infestations were not found before September, and from the size of the animals in the panels it was concluded that in the Port of Rotterdam area they spawned from August until the end of November. The settlement height was negatively correlated with the distance of the panels to the sea floor. In the first season after settlement they showed a substantial growth rate of 0.18 cm day −1. The longest shipworm found measured 36.8 cm after 4–5 months of growth after settlement. Infestations and growth were lower in oak than in fir wood. In 2006 the maximum consumption of wood by individuals settled in the same year in panels at the bottom accounted for 12.4%. Shell size and body length of the animal after the first season of growth showed a significant positive logarithmic relation. In both 2006 and 2007 a similar relation between the average boring tube diameter and the length of the animals was found. Lower river discharges leading to salinisation of the eastern part of the Port of Rotterdam area create conditions favourable for the shipworm, with serious consequences for the piles upon which the quays are built.