Lineage-specific molecular probing reveals novel diversity and ecological partitioning of haplosporidians

ISME Journal

Volumn 8, Issue 1, 2014, Pages 177-186

  Hartikainen, Hanna ^a   Ashford, Oliver S ^a   Berney, Cédric ^a   Okamura, Beth ^a   Feist, Stephen W ^b   Baker Austin, Craig ^b   Stentiford, Grant D ^b   Bass, David ^a  

^a DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^b CENTRE FOR ENVIRONMENT   (United Kingdom)

Author keywords

Ascetosporea; Bonamia; Haplosporidia; Haplosporidium; Minchinia; Urosporidium

Indexed keywords

BENTHIC ENVIRONMENT; BIVALVE; BRACKISH WATER; CLADISTICS; COMMERCIAL SPECIES; DATA SET; DISEASE PREVALENCE; GENETIC ANALYSIS; MARINE ENVIRONMENT; MOLECULAR ANALYSIS; POLYMERASE CHAIN REACTION; RISK FACTOR;

ARTICLE; BIODIVERSITY; CLASSIFICATION; DATA MINING; ECOLOGY; ECOSYSTEM; EUROPE; GENETICS; HAPLOSPORIDIA; MICROBIOLOGY; MOLECULAR PROBE; PHYLOGENY; PHYSIOLOGY;

BIODIVERSITY; DATA MINING; ECOLOGY; ECOSYSTEM; ENVIRONMENTAL MICROBIOLOGY; EUROPE; HAPLOSPORIDA; MOLECULAR PROBES; PHYLOGENY;

EUROPE; PANAMA [CENTRAL AMERICA]; SOUTH AFRICA;

ASCETOSPORA; BONAMIA (HAPLOSPORIDA); HAPLOSPORIDIA; HAPLOSPORIDIUM; INVERTEBRATA; MINCHINIA; MOLLUSCA; OSTREIDAE; RHIZARIA; UROSPORIDIUM;

EID: 84891152322     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.136     Document Type: Article

References (53)

1. Altekar G, Dwarkadas S, Huelsenbeck JP, Ronquist F. (2004). Parallel metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20: 407-415. (Pubitemid 38262773)
2. Arzul I, Langlade A, Chollet B, Robert M, Ferrand S, Omnes E et al. (2011). Can the protozoan parasite Bonamia ostreae infect larvae of flat oysters Ostrea edulis Vet Parasitol 179: 69-76.
3. Bass D, Cavalier-Smith T. (2004). Phylum-specific environmental DNA analysis reveals remarkably high global biodiversity of Cercozoa (Protozoa). Int J Syst Evol Microbiol 54: 2393-2404. (Pubitemid 39585435)
4. Bass D, Chao EEY, Nikolaev S, Yabuki A, Ishida K-i, Berney C et al. (2009). Phylogeny of novel naked filose and reticulose Cercozoa: Granofilosea cl. n. and Proteomyxidea revised. Protist 160: 75-109.
5. Bass D, Yabuki A, Santini S, Romac S, Berney C. (2012). Reticulamoeba is a long-branched Granofilosean (Cercozoa) that is missing from sequence databases. PLoS One 7: e49090.
6. Bearham D, Spiers Z, Raidal S, Jones JB, Nicholls PK. (2008). Detection of Minchinia sp., in rock oysters Saccostrea cuccullata (Born, 1778) using DNA probes. J Invertebr Pathol 97: 50-60. (Pubitemid 350235481)
7. Bearham D, Spiers ZB, Raidal SR, Jones JB, Nicholls PK. (2009). Detection of Minchinia occulta in samples of pearl oysters Pinctada maxima infected by Haplosporidium hinei. Aust Vet J 87: 430-437.
8. Berney C, Fahrni J, Pawlowski J. (2004). How many novel eukaryotic 'kingdoms' Pitfalls and limitations of environmental DNA surveys. BMC Biol 2: 13.
9. Bik HM, Porazinska DL, Creer S, Caporaso JG, Knight R, Thomas WK. (2012). Sequencing our way towards understanding global eukaryotic biodiversity. TREE 27: 233-243.
10. Blaxter M, Mann J, Chapman T, Thomas F, Whitton C, Floyd R et al. (2005). Defining operational taxonomic units using DNA barcode data. Phi Trans R Soc B 360: 1935-1943. (Pubitemid 44365054)
11. Brate J, Logares R, Berney C, Ree DK, Klaveness D, Jakobsen KS et al. (2010). Freshwater Perkinsea and marine-freshwater colonizations revealed by pyrosequencing and phylogeny of environmental rDNA. ISME J 4: 1144-1153.
12. Burreson EM, Ford SE. (2004). A review of recent information on the Haplosporidia, with special reference to Haplosporidium nelsoni (MSX disease). Aquat Living Resour 17: 499-517. (Pubitemid 40059483)
13. Canning EU, Okamura B. (2004). Biodiversity and evolution of the Myxozoa. Adv Parasitol 56: 43-131. (Pubitemid 37532271)
14. Carnegie RB, Burreson EM, Mike Hine P, Stokes NA, Audemard C, Bishop MJ et al. (2006). Bonamia perspora n. sp.(Haplosporidia), a parasite of the oyster Ostreola equestris, is the first Bonamia species known to produce spores. J Eukaryot Microbiol 53: 232-245. (Pubitemid 43990867)
15. Carnegie RB, Cochennec-Laureau N. (2004). Microcell parasites of oysters: Recent insights and future trends. Aquat Living Resour 17: 519.
16. Cavalier-Smith T, Chao EEY. (2003). Phylogeny of Choanozoa, Apusozoa, and other Protozoa and early eukaryote megaevolution. J Mol Evol 56: 540-563. (Pubitemid 36418983)
17. Colwell RK, Mao CX, Chang J. (2004). Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85: 2717-2727. (Pubitemid 39448246)
18. Dong LF, Smith CJ, Papaspyrou S, Stott A, Osborn AM, Nedwell DB. (2009). Changes in benthic denitrification, nitrate ammonification, and anammox process rates and nitrate and nitrite reductase gene abundances along an estuarine nutrient gradient (the Colne Estuary, United Kingdom). Appl Environ Microbiol 75: 3171-3179.
19. Elston RA, Kent ML, Wilkinson MT. (1987). Resistance of Ostrea edulis to Bonamia ostreae infection. Aquaculture 64: 237-242.
20. Flores BS, Siddall ME, Burreson EM. (1996). Phylogeny of the Haplosporidia (Eukaryota: Alveolata) based on small subunit ribosomal RNA gene sequence. J Parasit 82: 616-623. (Pubitemid 26271858)
21. Hall TA. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
22. Hawkins RJ, Purdy KJ. (2007). Genotypic distribution of an indigenous model microorganism along an estuarine gradient. FEMS 62: 187-194. (Pubitemid 47609661)
23. Howe AT, Bass D, Chao EE, Cavalier-Smith T. (2011). New genera, species, and improved phylogeny of Glissomonadida (Cercozoa). Protist 162: 710-722.
24. Jones MDM, Forn I, Gadelha C, Egan MJ, Bass D, Massana R et al. (2011). Discovery of novel intermediate forms redefines the fungal tree of life. Nature 474: 200-203.
25. Katoh K, Kuma K-i, Toh H, Miyata T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511-518. (Pubitemid 40360980)
26. Linton EW. (2005). MacGDE: genetic data environment for MacOS X. Software available athttp://www.msu.edu/ Blintone/macgde. Logares R, Audic S, Santini S, Pernice MC, de Vargas C, Massana R. (2012). Diversity patterns and activity of uncultured marine heterotrophic flagellates unveiled with pyrosequencing. ISME J 6: 1823-1833.
27. Longshaw M, Malham SK. (2012). A review of the infectious agents, parasites, pathogens and commensals of European cockles (Cerastoderma edule and C. glaucum). J Mar Biol Assoc UK 1: 1-21.
28. López-Garcia P, Vereshchaka A, Moreira D. (2006). Eukaryotic diversity associated with carbonates and fluid-seawater interface in Lost City hydrothermal field. Environ Microbiol 9: 546-554. (Pubitemid 46072140)
29. Miller MA, Pfeiffer W, Schwartz T. (2010). Gateway Computing Environments Workshop (GCE), 2010. IEEE pp 1-8.
30. Molloy DP, GiambA%Rini L, Stokes NA, Burreson EM, Ovcharenko MA. (2012). Haplosporidium raabei n. sp.(Haplosporidia): a parasite of zebra mussels, Dreissena polymorpha (Pallas, 1771). Parasitology 139: 463-477.
31. Moreira D, López-Garcia P. (2002). The molecular ecology of microbial eukaryotes unveils a hidden world. Trends Microb 10: 31-38. (Pubitemid 34075262)
32. Nardsi V, Arzul I, Cargini D, Mosca F, Calzetta A, Traversa D et al. (2011). Detection of Bonamia ostreae and B. exitiosa (Haplosporidia) in Ostrea edulis from the Adriatic Sea (Italy). Dis Aquat Org 89: 79-85.
33. Newman MW, Johnson CA, Pauley GB. (1976). A Minchinia-like haplosporidan parasitizing blue crabs, Callinectes sapidus. J Invertebr Pathol 27: 311-315.
34. Okamura B, Feist S. (2011). Emerging diseases in freshwater systems. Freshwater Biol 56: 627-637.
35. Pawlowski J, Audic S, Adl S, Bass D, Belbahri L, Berney C et al. (2013). CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLoS Biol 10: e1001419.
36. Perkins FO. (2000). An Illustrated Guide to the Protozoa. Vol. 1. Lee JJ, Leedale GF, Bradbury P (eds). Society of Protozoologists: Lawrence, Kansas, USA. pp 1328-1341.
37. Pichot Y, Comps M, Tige G, Grizel H, Rabouin MA. (1980). Recherches sur Bonamia ostreae gen. n. sp. n. parasite nouveau de l'huître plate Ostrea edulis L. Revue des Travaux de l'Institut des Pêches Maritimes 43: 131-140.
38. Reece KS, Siddall ME, Stokes NA, Burreson EM. (2004). Molecular phylogeny of the Haplosporidia based on two independent gene sequences. J Parasitol 90: 1111-1122. (Pubitemid 40247392)
39. Richards TA, Bass D. (2005). Molecular screening of freeliving microbial eukaryotes: diversity and distribution using a meta-analysis. Curr Opin Microbiol 8: 240-252. (Pubitemid 40813065)
40. Ronquist F, Huelsenbeck JP. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. (Pubitemid 37038874)
41. Seaby RMH, Henderson PA. (2007). Community Analysis Package 4.0. PISCES Conservation Ltd: Lymington, UK. p 154.
42. Seshadri R, Kravitz SA, Smarr L, Gilna P, Frazier M. (2007). CAMERA: a community resource for metagenomics. PLoS Biol 5: e75.
43. Siddall ME, Aguado MT. (2006). Molecular phylogenetic evidence of a haplosporidian parasite infecting the polychaete Syllis nipponica (Imajima, 1966). Parasitol Res 99: 309-312. (Pubitemid 44015119)
44. Skovgaard A, Daugbjerg N. (2008). Identity and systematic position of Paradinium poucheti and other paradinium- like parasites of marine copepods based on morphology and nuclear-encoded SSU rDNA. Protist 159: 401-413.
45. Stamatakis A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690. (Pubitemid 44642609)
46. Stamatakis A, Hoover P, Rougemont J. (2008). A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57: 758-771.
47. Stentiford GD, Bateman KS, Stokes NA, Carnegie RB. (2013). Haplosporidium littoralis sp. nov.: a crustacean pathogen within the Haplosporida (Cercozoa, Ascetosporea). Dis Aquat Org, Doi:10.3354/dao02619.
48. Stentiford GD, Feist SW, Bateman KS, Hine PM. (2004). Haemolymph parasite of the shore crab Carcinus maenas: pathology, ultrastructure and observations on crustacean haplosporidians. Dis Aquat Org 59: 57-68. (Pubitemid 39588309)
49. Stokes NA, Siddall ME, Burreson EM. (1995). Small subunit ribosomal RNA gene sequence of Minchinia teredinis (Haplosporidia: Haplosporidiidae) and a specific DNA probe and PCR primers for its detection. J Invertebr Pathol 65: 300-308.
50. Sun S, Chen J, Li W, Altintas I, Lin A, Peltier S et al. (2011). Community cyberinfrastructure for advanced microbial ecology research and analysis: The CAMERA resource. Nucleic Acids Res 39: D546-D551.
51. Utari HB, Senapin S, Jaengsanong C, Flegel TW, Kruatrachue M. (2012). A haplosporidian parasite associated with high mortality and slow growth in Penaeus (Litopenaeus) vannamei cultured in Indonesia. Aquaculture 366-367: 85-89.
52. Wuyts J, De Rijk P, Van de Peer Y, Pison G, Rousseeuw P, De Wachter R. (2000). Comparative analysis of more than 3000 sequences reveals the existence of two pseudoknots in area V4 of eukaryotic small subunit ribosomal RNA. Nucleic Acids Res 28: 4698-4708.
53. Wuyts J, Van de Peer Y, Winkelmans T, De Wachter R. (2002). The European database on small subunit ribosomal RNA. Nucleic Acids Res 30: 183-185. (Pubitemid 34679537)