Thiosocius teredinicola gen. nov., sp. nov., a sulfur-oxidizing chemolithoautotrophic endosymbiont cultivated from the gills of the giant shipworm, Kuphus polythalamius

Altamia, Marvin A.; Shipway, J. Reuben; Concepción, Gisela P.; Haygood, Margo G.; Distel, Daniel L.

doi:10.1099/ijsem.0.003143

Cited by 19 publications

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“…Most of the genomes and metagenomes are described here for the first time, or, in a few cases, previously reported genomes/metagenomes were resequenced/reassembled/reanalyzed (see Materials and Methods). Two bacterial genomes of T. turnerae T7901 and T. teredinicola 2141T and metagenomes of K. polythalamius were previously described (7,14,23). The resulting statistics and accession numbers are provided in Table S1A in the supplemental material, while specimen and strain origins, many of which had not been previously reported, are given in Table S1B.…”

Section: Resultsmentioning

confidence: 99%

“…(13), while Bankia setacea symbionts (indicated with "Bs" prefix) were obtained using the technique described previously by O'Connor et al (9). Sulfur-oxidizing symbionts were isolated using the protocol specified previously by Altamia et al (23). For this study, additional T. turnerae and novel cellulolytic symbionts from Philippine specimens (indicated with "PMS" prefix) were isolated (Table S1).…”

Section: Methodsmentioning

confidence: 99%

“…For example, K. polythalamius is often found in sediment habitats (as well as in wood) where its gill symbionts are crucial to sulfide oxidation and carry out carbon fixation (7,22). K. polythalamius lacks significant amounts of cellulolytic symbionts such as T. turnerae and instead contains Thiosocius teredinicola, which oxidizes sulfide and generates energy for the host (23). Other shipworms are found in solid rock and in seagrass (24,25).…”

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Secondary Metabolism in the Gill Microbiota of Shipworms (Teredinidae) as Revealed by Comparison of Metagenomes and Nearly Complete Symbiont Genomes

et al. 2020

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Shipworms play critical roles in recycling wood in the sea. Symbiotic bacteria supply enzymes that the organisms need for nutrition and wood degradation. Some of these bacteria have been grown in pure culture and have the capacity to make many secondary metabolites. However, little is known about whether such secondary metabolite pathways are represented in the symbiont communities within their hosts. In addition, little has been reported about the patterns of host-symbiont co-occurrence. Here, we collected shipworms from the United States, the Philippines, and Brazil and cultivated symbiotic bacteria from their gills. We analyzed sequences from 22 shipworm gill metagenomes from seven shipworm species and from 23 cultivated symbiont isolates. Using (meta)genome sequencing, we demonstrate that the cultivated isolates represent all the major bacterial symbiont species and strains in shipworm gills. We show that the bacterial symbionts are distributed among shipworm hosts in consistent, predictable patterns. The symbiotic bacteria harbor many gene cluster families (GCFs) for biosynthesis of bioactive secondary metabolites, only <5% of which match previously described biosynthetic pathways. Because we were able to cultivate the symbionts and to sequence their genomes, we can definitively enumerate the biosynthetic pathways in these symbiont communities, showing that ∼150 of ∼200 total biosynthetic gene clusters (BGCs) present in the animal gill metagenomes are represented in our culture collection. Shipworm symbionts occur in suites that differ predictably across a wide taxonomic and geographic range of host species and collectively constitute an immense resource for the discovery of new biosynthetic pathways corresponding to bioactive secondary metabolites. IMPORTANCE We define a system in which the major symbionts that are important to host biology and to the production of secondary metabolites can be cultivated. We show that symbiotic bacteria that are critical to host nutrition and lifestyle also have an immense capacity to produce a multitude of diverse and likely novel bioactive secondary metabolites that could lead to the discovery of drugs and that these pathways are found within shipworm gills. We propose that, by shaping associated microbial communities within the host, the compounds support the ability of shipworms to degrade wood in marine environments. Because these symbionts can be cultivated and genetically manipulated, they provide a powerful model for understanding how secondary metabolism impacts microbial symbiosis.

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confidence: 99%

Section: Methodsmentioning

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Secondary Metabolism in the Gill Microbiota of Shipworms (Teredinidae) as Revealed by Comparison of Metagenomes and Nearly Complete Symbiont Genomes

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“…Rather, K . polythalamius harbors sulfur-oxidizing chemoautotrophic (thioautotrophic) bacteria, indicating that these sediment-dwelling shipworms may be chemoautrophic; i.e., they exploit H 2 S as a source of nutritional energy [11, 39].…”

Section: Discussionmentioning

confidence: 99%

Shipworm bioerosion of lithic substrates in a freshwater setting, Abatan River, Philippines: Ichnologic, paleoenvironmental and biogeomorphical implications

et al. 2019

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Teredinid bivalves, commonly referred to as shipworms, are known for their propensity to inhabit, bioerode, and digest woody substrates across a range of brackish and fully marine settings. Shipworm body fossils and/or their borings, which are most allied with the ichnotaxon Teredolites longissimus, are found in wood preserved in sedimentary sequences ranging in age from Early Cretaceous to Recent and traditionally they have been regarded as evidence of marginal marine or marine depositional environments. Recent studies associated with the Philippine Mollusk Symbiont International Collaboration Biodiversity Group (PMS-ICBG) expedition on the island of Bohol, Philippines, have identified a new shipworm taxon (Lithoredo abatanica) that is responsible for macrobioerosion of a moderately indurated Neogene foraminiferal packstone cropping out along a freshwater reach of the Abatan River. In the process of drilling into and ingesting the limestone, these shipworms produce elongate borings that expand in diameter very gradually toward distal termini, exhibit sinuous or highly contorted axes and circular transverse outlines, and are lined along most of their length by a calcite tube. Given their strong resemblance to T. longissimus produced in wood but their unusual occurrence in a lithic substrate, these shipworm borings can be regarded as incipient Gastrochaenolites or, alternatively, as Apectoichnus. The alternate names reflect that the borings provide a testbed for ideas of the appropriateness of substrate as an ichnotaxobasis. The discovery of previously unrecognized shipworm borings in lithic substrates and the co-occurrence of another shipworm (Nausitora) in submerged logs in the same freshwater setting have implications for interpreting depositional conditions based on fossil teredinids or their ichnofossils. Of equal significance, the Abatan River study demonstrates that macrobioerosion in freshwater systems may be just as important as it is in marine systems with regard to habitat creation and landscape development. L. abatanica serve as ecosystems engineers in the sense that networks of their abandoned borings provide habitats for a variety of nestling invertebrates, and associated bioerosion undoubtedly enhances rates of mechanical and chemical degradation, thus influencing the Abatan River profile.

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“… T. turnerae is unusual among intracellular endosymbionts of marine taxa in that it is among the few that have been brought into pure culture. To our knowledge, T. turnerae is the only cellulolytic intracellular endosymbiont formally described to date, although a chemoautotrophic sulfur-oxidizing symbiont, Thiosocius teredinicola , from the gills of the giant sediment-dwelling shipworm Kuphus polythalamius has recently been described [ 2 ].…”

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Teredinibacter waterburyi sp. nov., a marine, cellulolytic endosymbiotic bacterium isolated from the gills of the wood-boring mollusc Bankia setacea (Bivalvia: Teredinidae) and emended description of the genus Teredinibacter

Altamia

Shipway

Stein

et al. 2020

International Journal of Systematic and Evolutionary Microbiology

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Thiosocius teredinicola gen. nov., sp. nov., a sulfur-oxidizing chemolithoautotrophic endosymbiont cultivated from the gills of the giant shipworm, Kuphus polythalamius

Cited by 19 publications

References 30 publications

Secondary Metabolism in the Gill Microbiota of Shipworms (Teredinidae) as Revealed by Comparison of Metagenomes and Nearly Complete Symbiont Genomes

Secondary Metabolism in the Gill Microbiota of Shipworms (Teredinidae) as Revealed by Comparison of Metagenomes and Nearly Complete Symbiont Genomes

Shipworm bioerosion of lithic substrates in a freshwater setting, Abatan River, Philippines: Ichnologic, paleoenvironmental and biogeomorphical implications

Teredinibacter waterburyi sp. nov., a marine, cellulolytic endosymbiotic bacterium isolated from the gills of the wood-boring mollusc Bankia setacea (Bivalvia: Teredinidae) and emended description of the genus Teredinibacter

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