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Symbiotic bacteria of helminths: what role may they play in ecosystems under anthropogenic stress?

Published online by Cambridge University Press:  12 January 2016

N.J. Morley
N.J. Morley*
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK
*
*E-mail: [email protected]
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Abstract

Symbiotic bacteria are a common feature of many animals, particularly invertebrates, from both aquatic and terrestrial habitats. These bacteria have increasingly been recognized as performing an important role in maintaining invertebrate health. Both ecto- and endoparasitic helminths have also been found to harbour a range of bacterial species which provide a similar function. The part symbiotic bacteria play in sustaining homeostasis of free-living invertebrates exposed to anthropogenic pressure (climate change, pollution), and the consequences to invertebrate populations when their symbionts succumb to poor environmental conditions, are increasingly important areas of research. Helminths are also susceptible to environmental stress and their symbiotic bacteria may be a key aspect of their responses to deteriorating conditions. This article summarizes the ecophysiological relationship helminths have with symbiotic bacteria and the role they play in maintaining a healthy parasite and the relevance of specific changes that occur in free-living invertebrate–bacteria interactions under anthropogenic pressure to helminths and their bacterial communities. It also discusses the importance of understanding the mechanistic sensitivity of helminth–bacteria relationships to environmental stress for comprehending the responses of parasites to challenging conditions.

Type
Review Article
Information
Journal of Helminthology , Volume 90 , Issue 6 , November 2016 , pp. 647 - 657
Copyright
Copyright © Cambridge University Press 2016 

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References

Aho, J.M., Uglem, G.L., Moore, J.P. & Larson, O.R. (1991) Bacteria associated with the tegument of Clinostomum marginatum (Digenea). Journal of Parasitology 77, 784–786.Google Scholar
Anderson, W.R., Tromba, F.G., Thompson, D.E. & Madden, P.A. (1973) Bacteriologic and histologic examination of Stephanurus dentatus parasitizing swine ureters. Journal of Parasitology 59, 765–769.Google Scholar
Apprill, A., Marlow, H.Q., Martindale, M.Q. & Rappe, M.S. (2009) The onset of microbial associations in the coral Pocillopora meandrina . ISME Journal 3, 685–699.CrossRefGoogle ScholarPubMed
Bakke, T.A., Cable, J. & Østbø, M. (2006) The ultrastructure of hypersymbionts on the monogenean Gyrodactylus salaris infecting Atlantic salmon Salmo salar . Journal of Helminthology 80, 377–386.Google Scholar
Baron, R.R., Hansen, M.F. & Lord, T.H. (1960) Bacterial flora of the roundworm Ascaridia galli Schrank and its relationship to the host flora. Experimental Parasitology 9, 281–292.Google Scholar
Bezerra, M., Vieira, E.C., Pleasants, J.R., Nicoli, J.R., Coelho, P.M.Z. & Bambirra, E.A. (1985) The life cycle of Schistosoma mansoni under germ free conditions. Journal of Parasitology 71, 519–520.Google Scholar
Bright, M. & Bulgheresi, S. (2010) A complex journey: transmission of microbial symbionts. Nature Reviews Microbiology 8, 218–230.Google Scholar
Brownlee, D.J.A., Fairweather, I., Johnston, C.F. & Shaw, C. (1994) Immunocytochemical demonstration of peptidergic and serotoninergic components in the enteric nervous system of the roundworm, Ascaris suum (Nematoda, Ascaroidea). Parasitology 108, 89–103.Google Scholar
Cable, J. & Tinsley, R.C. (1992) Microsporidian hyperparasites and bacteria associated with Pseudodiplorchis americanus (Monogenea: Polystomatidae). Canadian Journal of Zoology 70, 523–529.Google Scholar
Canning, E.U. (1975) The microsporidian parasites of Platyhelminthes: their morphology, development, transmission and pathogenicity. Commonwealth Institute of Helminthology Miscellaneous Publications 2, 1–32.Google Scholar
Chaston, J. & Goodrich-Blair, H. (2010) Common trends in mutualism revealed by model associations between invertebrates and bacteria. FEMS Microbiology Reviews 34, 41–58.Google Scholar
Company, R., Serafim, A., Cosson, R., Camus, L., Shillito, B., Fiala-Medioni, A. & Bebianno, M.J. (2006) The effect of cadmium on antioxidant responses and the susceptibility to oxidative stress in the hydrothermal vent mussel Bathymodiolus azoricus . Marine Biology 148, 817–825.CrossRefGoogle Scholar
Cusack, R. & Cone, D.K. (1985) A report of bacterial microcolonies on the surface of Gyrodactylus (Monogenea). Journal of Fish Diseases 8, 125–127.Google Scholar
Doll, J.P. & Franker, C.K. (1963) Experimental histomoniasis in gnotobiotic turkeys. I. Infection and histopathology of the bacteria-free host. Journal of Parasitology 49, 411–414.Google Scholar
Dollfus, R.Ph.F. (1946) Parasites (animaux et végétaux) des Helminthes. Encyclopedie Biologique 27, 1–482.Google Scholar
Douglas, A.E. (2007) Symbiotic microorganisms: untapped resources for insect pest control. Trends in Biotechnology 25, 338–342.CrossRefGoogle ScholarPubMed
Ehrlich, H.L. (1997) Microbes and metals. Applied Microbiology and Biotechnology 48, 687–692.Google Scholar
Emanuiloff, I. (1958) Untersuchung der wechselbeiziehungen zwischen bakterien und Ascariden in der darmparasitozönose bei schweinen und pferden. Zentralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene 172, 113–126.Google Scholar
Forst, S.F. & Clarke, D. (2002) Bacteria–nematode symbiosis. pp. 57–77 in Gaugler, R. (Ed.) Entomopathogenic nematology. Wallingford, CAB International.Google Scholar
Greiman, S.E., Tkach, V.V. & Vaughan, J.A. (2013) Transmission rates of the bacterial endosymbiont, Neorickettsia risticii, during the asexual reproduction phase of its digenean host, Plagiorchis elegans, within naturally infected Lymnaeid snails. Parasites & Vectors 6, 303.CrossRefGoogle ScholarPubMed
Grewal, P.S., Gaugler, R. & Shupe, C. (1996) Rapid changes in thermal sensitivity of entomopathogenic nematodes in response to selection at temperature extremes. Journal of Invertebrate Pathology 68, 65–73.Google Scholar
Grobusch, M.P., Komnila, M., Autenrieth, I., Mehlhorn, H. & Kremsner, P.G. (2003) No evidence of Wolbachia endosymbiosis with Loa loa and Mansonella perstans . Parasitology Research 90, 405–408.Google Scholar
Hayes, K.S., Bancroft, A.J., Goldrick, M., Portsmouth, C., Roberts, L.S. & Grencis, R.K. (2010) Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris . Science 328, 1391–1394.Google Scholar
Holm, J.B., Sorobetea, D., Kiilerich, P., Ramayo-Caldas, Y., Estelle, J., Ma, T., Madsen, L., Kristiansen, K. & Svensson-frej, M. (2015) Chronic Trichuris muris infection decreases diversity of the intestinal microbiota and concomitantly increases the abundance of Lactobacilli. PLoS One 10, e0125495.Google Scholar
Houser, B.B. & Burns, W.C. (1968) Experimental infection of gnotobiotic Tenebrio molitor and white rats with Hymenolepis diminuta (Cestoda: Cyclophyllidea). Journal of Parasitology 54, 69–73.CrossRefGoogle ScholarPubMed
Hsu, S.-C., Johansson, K.R. & Donahue, M.J. (1986) The bacterial flora of the intestine of Ascaris suum and 5-hydroxytryptamine production. Journal of Parasitology 72, 545–549.Google Scholar
Hudson, A.J. & Floate, K.D. (2009) Further evidence for the absence of bacteria in horsehair worms (Nematomorpha: Gordiidae). Journal of Parasitology 95, 1545–1547.Google Scholar
Hughes-Stamm, S.R., Cribb, T.H. & Jones, M.K. (1999) Structure of the tegument and ectocommensal microorganisms of Gyliauchen nahaensis (Digenea: Gyliauchenidae), an inhabitant of herbivorous fish of the Great Barrier Reef, Australia. Journal of Parasitology 85, 1047–1052.Google Scholar
Hussa, E.A. & Goodrich-Blair, H. (2013) It takes a village: ecological and fitness impacts of multipartite mutualism. Annual Review of Microbiology 67, 161–178.Google Scholar
Izvekova, G.I. (2005a) Hydrolytic activity of enzymes of microflora associated with digestive-transport surfaces of pike intestine and Triaenophorus nodulosus (Cestoda, Pseudophyllidea) parasitizing in it. Journal of Evolutionary Biochemistry and Physiology 41, 185–193.Google Scholar
Izvekova, G.I. (2005b) Activity of carbohydrases of symbiotic microflora and their role in processes of digestion of fish and their parasitizing cestodes (on the example of pike and Triaenophorus nodulosus). Journal of Evolutionary Biochemistry and Physiology 41, 406–414.Google Scholar
Izvekova, G.I. (2006a) Hydrolytic activity of enzymes produced by symbiotic microflora and its role in digestion processes of bream and its intestinal parasite Caryophyllaeus laticeps (Cestoda, Caryophyllidea). Biology Bulletin 33, 287–292.Google Scholar
Izvekova, G.I. (2006b) Trophic interactions in the system host (Eelpout Lota lota)– parasites (Eubothrium rugosum)–symbiotic microflora at hydrolysis of carbohydrate food components. Journal of Evolutionary Biochemistry and Physiology 42, 595–603.Google Scholar
Izvekova, G.I. & Komova, A.V. (2005) The role of α-amylase of symbiotic microflora in digestion by lower cestodes and their fish hosts. Biology Bulletin 32, 167–171.Google Scholar
Izvekova, G.I. & Lapteva, N.A. (2004) Microflora associated with the digestive-transport surfaces of fish and their parasitic cestodes. Russian Journal of Ecology 35, 176–180.Google Scholar
Izvekova, G.I., Izvekov, E.I. & Plotnikov, A.O. (2007) Symbiotic microflora in fishes of different ecological groups. Biology Bulletin 34, 610–618.Google Scholar
Korneva, J.V. (2008) Nanobacteria associated with mucous intestines of freshwater fishes and tegument of their parasites (Cestoda). Acta Parasitologica 53, 312–314.Google Scholar
Koyama, K. (2013) Evidence for bacteria-independent hatching of Trichuris muris eggs. Parasitology Research 112, 1537–1542.Google Scholar
Koyama, K. (2016) Bacteria-induced hatching of Trichuris muris eggs occurs without direct contact between eggs and bacteria. Parasitology Research, in press.Google Scholar
Krecek, R.C., Sayre, R.M., Els, H.J., Van Niekerk, J.P. & Malan, F.S. (1987) Fine structure of a bacterial community associated with Cyathostomes (Nematoda: Strongylidae) of zebras. Proceedings of the Helminthological Society of Washington 54, 212–219.Google Scholar
Kreisinger, J., Bastien, G., Hauffe, H.C., Marchesi, J. & Perkins, S.E. (2015) Interactions between multiple helminths and the gut microbiota in wild rodents. Philosophical Transactions of the Royal Society B 370, 20140295.Google Scholar
Kuz'mina, V.V. & Pervushina, K.A. (2003) The role of proteinases of the enteral microbiota in temperature adaptation of fish and helminths. Doklady Biological Sciences 391, 326–328.Google Scholar
Lasee, B.A. & Sutherland, D.R. (1993) Bacterial colonization of tegumental surfaces of Culaeatrema inconstans Lasee et al. 1988 (Digenea) from the brook stickleback, Culaea inconstans . Journal of Fish Diseases 16, 83–85.Google Scholar
Lemoine, N., Buell, N., Hill, A. & Hill, M. (2007) Assessing the utility of sponge microbial symbiont communities as models to study global climate change: a case study with Halichondria bowerbanki . pp. 419–425 in Custodio, M.R., Lobo-Hajdu, G., Hajdu, E. & Muricy, G. (Eds) Porifera research: Biodiversity, innovation and sustainability. Serie Livros, Museu Nacional, Rio de Janeiro, Brazil.Google Scholar
Lesser, M.P., Falcon, L.I., Rodriguez-Roman, A., Enriquez, S., Hoegh-Guldberg, O. & Iglesias-Prieto, R. (2007) Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa . Marine Ecology Progress Series 346, 143–152.Google Scholar
Lopez-Legentil, S., Erwin, P.M., Pawlik, J.R. & Song, B. (2010) Effects of sponge bleaching on ammonia-oxidizing Archaea: distribution and relative expression of ammonia monooxygenase genes associated with the barrel sponge Xestospongia muta . Microbial Ecology 60, 561–571.Google Scholar
MacLeod, C.D. & Poulin, R. (2012) Host–parasite interactions: a litmus test for ocean acidification? Trends in Parasitology 28, 365–369.Google Scholar
Marcogliese, D.J. (2001) Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 1331–1352.Google Scholar
Marcogliese, D.J. (2004) Parasites: small players with crucial roles in the ecological theatre. EcoHealth 1, 151–164.Google Scholar
McKenney, E.A., Williamson, L., Yoder, A.D., Rawls, J.F., Bilbo, S.D. & Parher, W. (2015) Alteration of the rat cecal microbiome during colonization with the helminth Hymenolepis diminuta . Gut Microbes 6, 182–193.Google Scholar
Melhem, R.F. & LoVerde, P.T. (1984) Mechanism of interaction of Salmonella and Schistosoma species. Infection and Immunity 44, 274–281.Google Scholar
Mettrick, D.F. & Podesta, R.B. (1974) Ecological and physiological aspects of helminth–host interactions in the mammalian gastrointestinal canal. Advances in Parasitology 12, 183–278.Google Scholar
Mills, C.A. (1980) Temperature-dependent survival and reproduction within populations of the ectoparasitic digenean Transversotrema patialense on the fish host. Parasitology 81, 91–102.Google Scholar
Möller, H. (1978) The effects of salinity and temperature on the development and survival of fish parasites. Journal of Fish Biology 12, 311–323.CrossRefGoogle Scholar
Moran, N.A. (2006) Symbiosis. Current Biology 16, R866–R871.Google Scholar
Morley, N.J. (2009) Environmental risk and toxicology of human and veterinary waste pharmaceutical exposure to wild aquatic host–parasite relationships. Environmental Toxicology and Pharmacology 27, 161–175.Google Scholar
Morley, N.J. (2012) The effects of radioactive pollution on the dynamics of infectious diseases in wildlife. Journal of Environmental Radioactivity 106, 81–97.Google Scholar
Neave, M.J., Streton-Joyce, C., Glasby, C.J., McGuiness, K.A., Parry, D.L. & Gibb, K.S. (2012) The bacterial community associated with the marine polychaete Ophelina sp. 1 (Annelida: Opheliidae) is altered by copper and zinc contamination in sediments. Microbial Ecology 63, 639–650.Google Scholar
Newton, L.C. & McKenzie, J.D. (1995) Echinoderms and oil pollution: a potential stress assay using bacterial symbionts. Marine Pollution Bulletin 31, 453–456.Google Scholar
Newton, W.L., Weinstein, P.P. & Jones, M.F. (1959) A comparison of the development of some rat and mouse helminths in germfree and conventional guinea pigs. Annals of the New York Academy of Sciences 78, 290–306.CrossRefGoogle ScholarPubMed
Ottens, H. & Dickerson, G. (1972) Studies on the effects of bacteria on experimental schistosome infections in animals. Transactions of the Royal Society of Tropical Medicine and Hygiene 66, 85–107.Google Scholar
Pappas, P.W. & Read, C.P. (1975) Membrane transport in helminth parasites: a review. Experimental Parasitology 37, 469–530.Google Scholar
Philips, J.L., Sturman, G. & West, G.B. (1975) The presence of histamine in the tissues of Ascaris suum . General Pharmacology 6, 295–297.Google Scholar
Plotnikov, A.O. & Korneva, Zh.V. (2008) Morphological and ultrastructural characteristics of symbiotic bacteria colonizing the surface of the helminth Trianophorus nodulosus and the intestine of pike Esox lucius . Inland Water Biology 1, 25–31.Google Scholar
Poddubnaya, L.G. & Izvekova, G.I. (2005) Detection of bacteria associated with the tegument of caryophyllidean cestodes. Helminthologia 42, 9–14.Google Scholar
Podesta, R.B. & Mettrick, D.F. (1974) Components of glucose transport in the host parasite system Hymenolepis diminuta (Cestoda) and the rat intestine. Canadian Journal of Physiology and Pharmacology 52, 183–197.Google Scholar
Poinar, G.O., Thomas, G.M. & Lighthart, B. (1990) Bioassay to determine the effect of commercial preparations of Bacillus thuringiensis on entomogenous Rhabditoid nematodes. Agriculture, Ecosystems and Environment 30, 195–202.Google Scholar
Przyjalkowski, Z. (1977) Establishment, growth and rate of expulsion of the cestode Hymenolepis nana Siebold, 1882 in germfree and conventional mice. Acta Parasitologica Polonica 25, 63–68.Google Scholar
Reid, W.M. & Botero, H. (1967) Growth of the cestode Raillietina cesticillus in bacteria-free chickens. Experimental Parasitology 21, 149–153.Google Scholar
Reynolds, L.A., Smith, K.A., Filbey, K.J., Harcus, Y., Hewitson, J.P., Redpath, S.A., Valdez, Y., Yebra, M.J., Finlay, B.B. & Maizels, R.M. (2014) Commensal-pathogen interactions in the intestinal tract. Gut Microbes 5, 522–532.Google Scholar
Riggs, M.R., Lemly, A.D. & Esch, G.W. (1987) The growth, biomass, and fecundity of Bothriocephalus acheilognathi in a North Carolina cooling reservoir. Journal of Parasitology 73, 893–900.Google Scholar
Ritchie, K.B. (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Marine Ecology Progress Series 322, 1–14.Google Scholar
Schmitt, S., Weisz, J.B., Lindquist, N. & Hentschel, U. (2007) Vertical transmission of a phylogentically complex microbial consortium in the viviparous sponge Ircinia felix . Applied and Environmental Microbiology 73, 2067–2078.Google Scholar
Schmitt, S., Tsai, P., Bell, J., Fromont, J., Ilan, M., Lindquist, N., Perez, T., Rodrigo, A., Schupp, P.J., Vacelet, J., Webster, N., Hentschel, U. & Taylor, M.W. (2011) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME Journal 6, 564–576.Google Scholar
Sebelova, S., Kuperman, B. & Gelnar, M. (2002) Abnormalities of the attachment clamps of representatives of the family Diplozoidae. Journal of Helminthology 76, 249–259.Google Scholar
Selvin, J., Priya, S.S., Kiran, G.S., Thangavelu, T. & Bai, N.S. (2009) Sponge-associated marine bacteria as indicators of heavy metal pollution. Microbiological Research 164, 352–363.Google Scholar
Shahkolahi, A.M. & Donahue, M.J. (1993) Bacterial flora, a possible source of serotonin in the intestine of adult female Ascaris suum . Journal of Parasitology 79, 17–22.Google Scholar
Sharp, K.H. & Ritchie, K.B. (2012) Multi-partner interactions in corals in the face of climate change. Biological Bulletin 223, 66–77.Google Scholar
Silva, C.A.R. e, Smith, B.D. & Rainbow, P.S. (2006) Comparative biomonitors of coastal trace metal contamination in tropical South America (N. Brazil). Marine Environmental Research 61, 439–455.Google Scholar
Smith, L.D., Negri, A.P., Philip, E., Webster, N.S. & Heyward, A.J. (2003) The effects of antifoulant-paint-contaminated sediments on coral recruits and branchlets. Marine Biology 143, 651–657.Google Scholar
Stefanski, W. (1965) Bacterial flora as one of the ecological factors affecting the establishment of parasites in the intestines of their hosts. Acta Parasitologica Polonica 13, 1–6.Google Scholar
Stefanski, W. & Przyjalkowski, Z. (1965) Effect of alimentary tract microorganisms on the development of Trichinella spiralis in mice. Part I. Experimental Parasitology 16, 167–173.CrossRefGoogle Scholar
Stefanski, W. & Przyjalkowski, Z. (1966) Effect of alimentary tract microorganisms on the development of Trichinella spiralis in mice. Part II. Experimental Parasitology 18, 92–98.Google Scholar
Sures, B. (2003) Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 126, S53–S60.Google Scholar
Syvokienë, J. & Mickënienë, L. (1999) Micro-organisms in the digestive tract of fish as indicators of feeding conditions and pollution. ICES Journal of Marine Science 56, 147–149.Google Scholar
Taylor, M.J., Bandi, C. & Hoerauf, A. (2005) Wolbachia bacterial endosymbionts of filarial nematodes. Advances in Parasitology 60, 245–284.Google Scholar
Taylor, M., Mediannikov, O., Raoult, D. & Greub, G. (2012) Endosymbiotic bacteria associated with nematodes, ticks and amoebae. FEMS Immunology and Medical Microbiology 64, 21–31.CrossRefGoogle ScholarPubMed
Tian, R.-M., Wang, Y., Bougouffa, S., Gao, Z.-M., Cai, L., Zhang, W.-P., Bajic, V. & Qian, P.-Y. (2014a) Effect of copper treatment on the composition and function of the bacterial community in the sponge Haliclona cymaeformis . mBio 5, e01980–e01914.Google Scholar
Tian, R.M., Lee, O.O., Wang, Y., Cai, L., Bougouffa, S., Chiu, J.M.Y., Wu, R.S.S. & Qian, P.-Y. (2014b) Effect of polybrominated diphenyl ether (PBDE) treatment on the composition and function of the bacterial community in the sponge Haliclona cymaeformis . Frontiers in Microbiology 5, 799.Google Scholar
Tuazon, C.U., Nash, T., Cheever, A. & Neva, F. (1985) Interaction of Schistosoma japonicum with Salmonellae and other gram-negative bacteria. Journal of Infectious Diseases 152, 722–726.Google Scholar
Uglem, G.L., Larson, O.R., Aho, J.M. & Lee, K.J. (1991) Fine structure and sugar transport functions of the tegument in Clinostomum marginatum (Digenea: Clinostomatidae): environmental effects on the adult phenotype. Journal of Parasitology 77, 658–662.Google Scholar
Vaughan, J.A., Tkach, V.V. & Greiman, S.E. (2012) Neorickettsial endosymbionts of the Digenea: diversity, transmission and distribution. Advances in Parasitology 79, 253–297.Google Scholar
Vejzagić, N., Adelfio, R., Keiser, J., Kringel, H., Thamsborg, S.M. & Kapal, C.M.O. (2015) Bacteria-induced egg hatching differs for Trichuris muris and Trichuris suis . Parasites & Vectors 8, 371.Google Scholar
Vidal-Martinez, V.M., Pech, D., Sures, B., Purucker, S.T. & Poulin, R. (2010) Can parasites really reveal environmental impact? Trends in Parasitology 26, 44–51.Google Scholar
Walk, S.T., Blum, A.M., Ewing, S.A.-S., Weinstock, J.V. & Young, V.B. (2010) Alteration of the murine gut microbiota during infection with the parasitic helminth, Heligmosomoides polygyrus . Inflammatory Bowel Diseases 16, 1841–1849.Google Scholar
Webster, J.M., Chen, G., Hu, K. & Li, J. (2002) Bacterial metabolites. pp. 99–114 in Gaugler, R. (Ed.) Entomopathogenic nematology. Wallingford, CAB International.Google Scholar
Webster, N.S. & Blackall, L.L. (2009) What do we really know about sponge-microbial symbioses? ISME Journal 3, 1–3.Google Scholar
Webster, N.S. & Taylor, M.W. (2012) Marine sponges and their microbial symbionts: love and other relationships. Environmental Microbiology 14, 335–346.Google Scholar
Webster, N.S., Webb, R.I., Ridd, M.J., Hill, R.T. & Negri, A.P. (2001) The effects of copper on the microbial community of a coral reef sponge. Environmental Microbiology 3, 19–31.Google Scholar
Webster, N.S., Cobb, R.E. & Negri, A.P. (2008) Temperature thresholds for bacterial symbiosis with a sponge. ISME Journal 2, 830–842.Google Scholar
Webster, N.S., Botte, E.S., Soo, R.M. & Whelan, S. (2011) The larval sponge holobiont exhibits high thermal tolerance. Environmental Microbiology Reports 3, 756–762.Google Scholar
Webster, N.S., Negri, A.P., Flores, F., Humphrey, C., Soo, R., Botte, E.S., Vogel, N. & Uthicke, S. (2013) Near-future ocean acidification causes differences in microbial associations within diverse coral reef taxa. Environmental Microbiology Reports 5, 243–251.Google Scholar
Weinstein, P.P., Newton, W.I., Sawyer, T.K. & Sommerville, R.I. (1969) Nematospiroides dubius: development and passage in the germfree mouse, and a comparative study of the free-living stages in germfree feces and conventional culture. Transactions of the American Microscopical Society 88, 95–117.Google Scholar
Wescott, R.B. (1970) Metazoa–Protozoa–bacteria interrelationships. American Journal of Clinical Nutrition 23, 1502–1507.Google Scholar
Zhou, X., Kaya, H.K., Heungens, K. & Goodrich-Blair, H. (2002) Response of ants to deterrent factor(s) produced by the symbiotic bacteria of entomopathogenic nematodes. Applied Environmental Microbiology 68, 6202–6209.Google Scholar
Ziino, G., Giuffrida, S., Bilei, S. & Panebianco, A. (2009) Bacteria isolated from 25 hydatid cysts in sheep, cattle and goats. Veterinary Record 165, 234–236.Google Scholar