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Bacterial and archaeal communities inhabiting mussels, sediment and water in Indonesian anchialine lakes

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Abstract

Anchialine lakes are a globally rare and unique ecosystem consisting of saline lakes surrounded by land and isolated from the surrounding marine environment. These lakes host a unique flora and fauna including numerous endemic species. Relatively few studies have, however, studied the prokaryote communities present in these lakes and compared them with the surrounding ‘open water’ marine environment. In the present study, we used a 16S rRNA gene barcoded pyrosequencing approach to examine prokaryote (Bacteria and Archaea) composition in three distinct biotopes (sediment, water and the mussel Brachidontes sp.) inhabiting four habitats, namely, three marine lakes and the surrounding marine environment of Berau, Indonesia. Biotope and habitat proved significant predictors of variation in bacterial and archaeal composition and higher taxon abundance. Most bacterial sequences belonged to OTUs assigned to the Proteobacteria. Compared to sediment and water, mussels had relatively high abundances of the classes Mollicutes and Epsilonproteobacteria. Most archaeal sequences, in turn, belonged to OTUs assigned to the Crenarchaeota with the relative abundance of crenarchaeotes highest in mussel samples. For both Bacteria and Archaea, the main variation in composition was between water samples on the one hand and sediment and mussel samples on the other. Sediment and mussels also shared much more OTUs than either shared with water. Abundant bacterial OTUs in mussels were related to organisms previously obtained from corals, oysters and the deepsea mussel Bathymodiolus manusensis. Abundant archaeal OTUs in mussels, in contrast, were closely related to organisms previously obtained from sediment.

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References

  • Aguirre ML, Perez SI, Sirch YN (2006) Morphological variability of Brachidontes swainson (Bivalvia, Mytilidae) in the marine Quaternary of Argentina (SW Atlantic). Palaeogeogr Palaeoclimatol Palaeoecol 239:100–125. doi:10.1016/j.palaeo.2006.01.019

    Article  Google Scholar 

  • Alonso-Sáez L, Sánchez O, Gasol JM, Balagué V, Pedrós-Alio C (2008) Winter-to-summer changes in the composition and single-cell activity of near-surface Arctic prokaryotes. Environ Microbiol 10:2444–2454

    Article  PubMed  CAS  Google Scholar 

  • Assié A, Borowski C, van der Heijden K, Raggi L, Geier B, Leisch N et al (2016) A specific and widespread association between deep-sea Bathymodiolus mussels and a novel family of Epsilonproteobacteria. Env Microbiol Rep 8:805–813. doi:10.1111/1758-2229.12442

    Article  Google Scholar 

  • Becking LE, Renema W, Santodomingo NK, Hoeksema BW, Tuti Y, de Voogd NJ (2011) Recently discovered landlocked basins in Indonesia reveal high habitat diversity in anchialine systems. Hydrobiologia 677:89–105. doi:10.1007/s10750-011-0742-0

    Article  CAS  Google Scholar 

  • Becking LE, Cleary DFR, de Voogd NJ (2013) Sponge species composition, abundance, and cover in marine lakes and coastal mangroves in Berau, Indonesia. Mar Ecol Prog Ser 481:105–120. doi:10.3354/meps10155

    Article  Google Scholar 

  • Becking LE, de Leeuw C, Vogler C (2014) Newly discovered” jellyfish lakes” in Misool, Raja Ampat, Papua, Indonesia. Mar Biodivers 45:597–598

    Article  Google Scholar 

  • Becking LE, de Leeuw CA, Knegt B, Maas DL, De Voogd NJ, Suyatna I, Peijnenburg KT (2016) Highly divergent mussel lineages in isolated Indonesian marine lakes. PeerJ 4:e2496

    Article  PubMed  PubMed Central  Google Scholar 

  • Bowen JL, Morrison HG, Hobbie JE, Sogin ML (2012) Salt marsh sediment diversity: a test of the variability of the rare biosphere among environmental replicates. ISME J 6:2014–2023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brenner M, Ramdohr S, Effkemann S, Stede M (2009) Key parameters for the consumption suitability of offshore cultivated blue mussels (Mytilus edulis L.) in the German Bight. Eur Food Res Technol 230:255–267

    Article  CAS  Google Scholar 

  • Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252

    Article  CAS  PubMed  Google Scholar 

  • Brochier-Armanet C, Gribaldo S, Forterre P (2012) Spotlight on the Thaumarchaeota. ISME J 6:227

    Article  CAS  PubMed  Google Scholar 

  • Buschbaum C, Dittmann S, Hong JS, Hwang IS, Strasser M, Thiel M et al (2008) Mytilid mussels: global habitat engineers in coastal sediments. Helgol Mar Res 63:47

    Article  Google Scholar 

  • Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile ε-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468. doi:10.1038/nrmicro141

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caston CB, Nowlin WH, Gaulke A, Vanni MJ (2009) The relative importance of heterotrophic bacteria to pelagic ecosystem dynamics varies with reservoir trophic state. Limnol Oceanogr 54:2143–2156

    Article  Google Scholar 

  • Cato EP, George WL, Finegold SM (1986) Genus Clostridium. In: Sneath PHA (ed) Bergey’s manual of systematic bacteriology. Williams and Wilkins, Baltimore, pp 1141–1200

    Google Scholar 

  • Cerrano C, Azzini F, Bavestrello G, Calcinai B, Pansini M, Sarti M, Thung D (2006) Marine lakes of karst islands in Ha Long Bay (Vietnam). Chem Ecol 22:489–500

    Article  Google Scholar 

  • Charlson RJ, Lovelock JE, Andreae MO, Warren SG (1987) Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326:655–661

    Article  CAS  Google Scholar 

  • Chen JS (2004) Nitrogen fixation in Clostridia. In: Klipp W, Masepohl B, Gallon JR, Newton WE (eds) Genetics and regulation of nitrogen fixation in free-living bacteria. Kluwer Academic Publishers, Dordrecht, pp 53–62

    Google Scholar 

  • Cleary DFR (2003) An examination of scale of assessment, logging and ENSO-induced fires on butterfly diversity in Borneo. Oecologia 135:313–321

    Article  PubMed  Google Scholar 

  • Cleary DFR, Becking LE, Voogd NJ, Pires AC, Polónia ARM, Egas C, Gomes NCM (2013) Habitat-and host-related variation in sponge bacterial symbiont communities in Indonesian waters. FEMS Microbiol Ecol 85:465–482

    Article  CAS  PubMed  Google Scholar 

  • Cleary DFR, Becking LE, Polónia ARM, Freitas RM et al (2015a) Composition and predicted functional ecology of mussel-associated bacteria in Indonesian marine lakes. A van Leeuw J Microb 107:821–834. doi:10.1007/s10482-014-0375-1

    Article  Google Scholar 

  • Cleary DFR, de Voogd NJ, Polónia ARM, Freitas RM et al (2015b) Composition and predictive functional analysis of bacterial communities in seawater, sediment and sponges in the Spermonde Archipelago, Indonesia. Microb Ecol 70:889

    Article  CAS  PubMed  Google Scholar 

  • Cock PJ, Antao T, Chang JT, Chapman BA, Cox CJ, Dalke A et al (2009) Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25:1422–1423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colin PL (2009) Marine environments of Palau. Indo-Pacific Press, San Diego

    Google Scholar 

  • Currie DJ, Kalff J (1984) The relative importance of bacterioplankton and phytoplankton in phosphorus uptake in freshwater. Limnol Oceanogr 29:311–321

    Article  CAS  Google Scholar 

  • Dang H, Zhou H, Yang J, Ge H, Jiao N, Luan X et al (2013) Thaumarchaeotal signature gene distribution in sediments of the northern South China Sea: an indicator of the metabolic intersection of the marine carbon, nitrogen, and phosphorus cycles? Appl Environ Microb 79:2137–2147

    Article  CAS  Google Scholar 

  • Danger M, Oumarou C, Benest D, Lacroix G (2007) Bacteria can control stoichiometry and nutrient limitation of phytoplankton. Funct Ecol 21:202–210

    Article  Google Scholar 

  • de Voogd NJ, Cleary DFR, Polónia ARM, Gomes NCM (2015) Bacterial community composition and predicted functional ecology of sponges, sediment and seawater from the thousand islands reef complex, West Java, Indonesia. FEMS Microbiol Ecol 91:fiv019. doi:10.1093/femsec/fiv019

    Article  PubMed  CAS  Google Scholar 

  • DiTullio GR, Grebmeier JM, Arrigo KR, Lizotte MP, Robinson DH, Leventer A et al (2000) Rapid and early export of Phaeocystis antarctica blooms in the Ross Sea, Antarctica. Nature 404:595–598

    Article  CAS  PubMed  Google Scholar 

  • Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6:725–740

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feldman SH, Wimsatt J, Marchang RE, Johnson AJ, Brown W, Mitchell JC, Sleeman J (2006) A novel mycoplasma detected in association with upper respiratory disease syndrome in free-ranging eastern box turtles (Terrapene carolina carolina) in Virginia. J Wildl Dis 42:279–289

    Article  CAS  PubMed  Google Scholar 

  • Frank KL, Rogers DR, Olins HC, Vidoudez C, Girguis PR (2013) Characterizing the distribution and rates of microbial sulfate reduction at Middle Valley hydrothermal vents. ISME J 7:1391–1401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frigaard NU, Martinez A, Mincer TJ, DeLong EF (2006) Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439:847–850

    Article  CAS  PubMed  Google Scholar 

  • Gaidos E, Rusch A, Ilardo M (2011) Ribosomal tag pyrosequencing of DNA and RNA from benthic coral reef microbiota: community spatial structure, rare members and nitrogen-cycling guilds. Environ Microbiol 13:1138–1152

    Article  PubMed  Google Scholar 

  • Galand PE, Lovejoy C, Vincent WF (2006) Remarkably diverse and contrasting archaeal communities in a large arctic river and the coastal Arctic Ocean. Aquat Microb Ecol 44:115–126

    Article  Google Scholar 

  • Galand PE, Lovejoy C, Pouliot J, Vincent WF (2008) Heterogeneous archaeal communities in the particle-rich environment of an arctic shelf ecosystem. J Mar Syst 74:774–782

    Article  Google Scholar 

  • Galitskaya P, Akhmetzyanova L, Selivanovskaya S (2016) Biochar-carrying hydrocarbon decomposers promote degradation during the early stage of bioremediation. Biogeosciences 13:5739

    Article  Google Scholar 

  • Ginzburg B, Chalifa I, Gun J, Dor I, Hadas O, Lev O (1998) DMS formation by dimethylsulfoniopropionate route in freshwater. Environ Sci Technol 32:2130–2136

    Article  CAS  Google Scholar 

  • Goffredi SK (2010) Indigenous ectosymbiotic bacteria associated with diverse hydrothermal vent invertebrates. Environ Microbiol Rep 2:479–488

    Article  PubMed  Google Scholar 

  • Gomes NCM, Heuer H, Schönfeld J, Costa R, Mendonca-Hagler L, Smalla K (2001) Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 232:167–180

    Article  CAS  Google Scholar 

  • Goto TV, Tamate HB, Hanzawa N (2011) Phylogenetic characterization of three morphs of mussels (Bivalvia, Mytilidae) inhabiting isolated marine environments in Palau Islands. Zool Sci 28:568–579. doi:10.2108/zsj.28.568

    Article  CAS  PubMed  Google Scholar 

  • Hardoim CC, Costa R (2014) Temporal dynamics of prokaryotic communities in the marine sponge Sarcotragus spinosulus. Mol Ecol 23:3097–3112

    Article  CAS  PubMed  Google Scholar 

  • Harshbarger JC, Chang SC (1977) Chlamydiae (with phages), mycoplasmas, and richettsiae in Chesapeake Bay bivalves. Science 196:666–668

    Article  CAS  PubMed  Google Scholar 

  • Hoeksema BW (2004) Marine biodiversity of the coastal area of the Berau region, East Kalimantan, Indonesia: pro gress report East Kalimantan program—pilot phase (October 2003). Naturalis, Leiden

  • Holben WE, Williams P, Saarinen M, Särkilahti LK, Apajalahti JHA (2002) Phylogenetic analysis of intestinal microflora indicates a novel Mycoplasma phylotype in farmed and wild salmon. Microb Ecol 44:175–185

    Article  CAS  PubMed  Google Scholar 

  • Holthuis LB (1973) Caridean shrimps found in land-locked saltwater pools at four Indo-West Pacific localities (Sinai Peninsula, Funafuti Atoll, Maui and Hawaii Islands): with the description of one new genus and four new species. Brill

  • Iverson V, Morris RM, Frazar CD, Berthiaume CT, Morales RL, Armbrust EV (2012) Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota. Science 335:587–590

    Article  CAS  PubMed  Google Scholar 

  • King GM, Judd C, Kuske CR, Smith C (2012) Analysis of stomach and gut microbiomes of the eastern oyster (Crassostrea virginica) from coastal Louisiana, USA. PLoS ONE 7:e51475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Könneke M, Bernhard AE, José R, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    Article  PubMed  CAS  Google Scholar 

  • Lee T, Foighil DÓ (2004) Hidden Floridian biodiversity: mitochondrial and nuclear gene trees reveal four cryptic species within the scorched mussel, Brachidontes exustus, species complex. Mol Ecol 13:3527–3542

    Article  CAS  PubMed  Google Scholar 

  • Lee T, Foighil DÓ (2005) Placing the Floridian marine genetic disjunction into a regional evolutionary context using the scorched mussel, Brachidontes exustus, species complex. Evolution 59:2139–2158. doi:10.1111/j.1365-294X.2004.02337.x

    Article  CAS  PubMed  Google Scholar 

  • Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280

    Article  PubMed  Google Scholar 

  • Li X, Yan Q, Ringø E, Wu X, He Y, Yang D (2016) The influence of weight and gender on intestinal bacterial community of wild largemouth bronze gudgeon (Coreius guichenoti, 1874). BMC Microbiol 16:191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lincoln SA, Wai B, Eppley JM, Church MJ, Summons RE, DeLong EF (2014a) Planktonic Euryarchaeota are a significant source of archaeal tetraether lipids in the ocean. Proc Natl Acad Sci USA 111:9858–9863. doi:10.1073/pnas.1409439111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lincoln SA, Wai B, Eppley JM, Church MJ, Summons RE, DeLong EF (2014b) Reply to Schouten et al.: Marine Group II planktonic Euryarchaeota are significant contributors to tetraether lipids in the ocean. Proc Natl Acad Sci USA 111:E4286. doi:10.1073/pnas.1416736111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Zhang CL, Yang C, Chen S, Cao Z, Zhang Z, Tian J (2017) Marine Group II Dominates Planktonic Archaea in Water Column of the Northeastern South China Sea. Front Microbio 8:1098

    Article  Google Scholar 

  • Loggans DE, Biesiot PM, Wang SY (2006) Gut microbial communities in the estuarine bivalves Geukensia demissa and Crassostrea virginica. Integr Comp Biol 46:E223

    Google Scholar 

  • Maciolek J (1983) Distribution and biology of Indo-Pacific insular hypogeal shrimps. B Mar Sci 33:606–618

    Google Scholar 

  • Martin-Cuadrado AB, Garcia-Heredia I, Molto AG, Lopez-Ubeda R, Kimes N, López-García P et al (2015) A new class of marine Euryarchaeota group II from the mediterranean deep chlorophyll maximum. ISME J 9:1619–1634

    Article  CAS  PubMed  Google Scholar 

  • Martínez-García M, Stief P, Díaz-Valdés M, Wanner G, Ramos-Esplá A, Dubilier N, Antón J (2008) Ammonia-oxidizing Crenarchaeota and nitrification inside the tissue of a colonial ascidian. Environ Microbiol 10:2991–3001

    Article  PubMed  CAS  Google Scholar 

  • Massana R, DeLong EF, Pedrós-Alió C (2000) A few cosmopolitan phylotypes dominate planktonic archaeal assemblages in widely different oceanic provinces. Appl Environ Microb 66:1777–1787

    Article  CAS  Google Scholar 

  • Massin C, Tomascik T (1996) Two new holothurians (Echinodermata: Holothuroidea) from an anchialine lagoon of an uplifted atoll, Kakaban Island, East Kalimantan, Indonesia. Raffles B Zool 44:157–172

    Google Scholar 

  • Meyer B, Kuever J (2007) Molecular analysis of the diversity of sulfate-reducing and sulfur-oxidizing prokaryotes in the environment, using aprA as functional marker gene. Appl Environ Microb 73:7664–7679. doi:10.1128/AEM.01272-07

    Article  CAS  Google Scholar 

  • Meyerhof MS, Wilson JM, Dawson MN, Michael Beman J (2016) Microbial community diversity, structure and assembly across oxygen gradients in meromictic marine lakes, Palau. Environ Microbiol 18:4907–4919

    Article  CAS  PubMed  Google Scholar 

  • Monteiro-Ribas W, Rocha-Miranda F, Romano RC, Quintanilha J (2006) Larval development of Brachidontes solisianus (Bivalvia, Mytilidae): with notes on differences between its hinge system and that of the mollusk Perna perna. Braz J Biol 66:109–116

    Article  CAS  PubMed  Google Scholar 

  • Offre P, Spang A, Schleper C (2013) Archaea in biogeochemical cycles. Annu Rev Microbiol 67:437–457

    Article  CAS  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Szoecs E, Wagner H (2017) vegan: Community Ecology Package. R package version 2.4-3. https://CRAN.R-project.org/package=vegan

  • Orsi WD, Smith JM, Liu S, Liu Z, Sakamoto CM, Wilken S et al (2016) Diverse, uncultivated bacteria and archaea underlying the cycling of dissolved protein in the ocean. ISME J 10:2158–2173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paillard C, Le Roux F, Borrego JJ (2004) Bacterial disease in marine bivalves, a review of recent studies: trends and evolution. Aquat Living Resour 17:477–498

    Article  Google Scholar 

  • Papazisi L, Gorton TS, Kutish G, Markham PF, Browning GF, Swartzell S et al (2003) The complete genome sequence of the avian pathogen Mycoplasma gallisepticum strain Rlow. Microbiology 149:2307–2316

    Article  CAS  PubMed  Google Scholar 

  • Petersen JM, Ramette A, Lott C, Cambon-Bonavita MA, Zbinden M, Dubilier N (2010) Dual symbiosis of the vent shrimp Rimicaris exoculata with filamentous gamma- and epsilonproteobacteria at four Mid-Atlantic Ridge hydrothermal vent fields. Environ Microbiol 12:2204–2218

    CAS  PubMed  Google Scholar 

  • Pfister CA, Meyer F, Antonopoulos DA (2010) Metagenomic profiling of a microbial assemblage associated with the California mussel: a node in networks of carbon and nitrogen cycling. PLoS ONE 5:e10518

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pires AC, Cleary DFR, Almeida A, Cunha Â, Dealtry S, Mendonça-Hagler LC et al (2012) Denaturing gradient gel electrophoresis and barcoded pyrosequencing reveal unprecedented archaeal diversity in mangrove sediment and rhizosphere samples. Appl Environ Microb 78:5520–5528. doi:10.1128/AEM.00386-12

    Article  CAS  Google Scholar 

  • Polónia ARM, Cleary DFR, Duarte LN, de Voogd NJ et al (2014) Composition of Archaea in seawater, sediment, and sponges in the Kepulauan Seribu Reef System, Indonesia. Microb Ecol 67:553

    Article  PubMed  Google Scholar 

  • Polónia ARM, Cleary DFR, Freitas R, Voogd NJ, Gomes NCM (2015) The putative functional ecology and distribution of archaeal communities in sponges, sediment and seawater in a coral reef environment. Mol Ecol 24:409–423

    Article  PubMed  CAS  Google Scholar 

  • Preston CM, Wu KY, Molinski TF, DeLong EF (1996) A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc Natl Acad Sci USA 93:6241–6246. doi:10.1073/pnas.93.13.6241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available from http://www.R-project.org/

  • Reigstad LJ, Richter A, Daims H, Urich T, Schwark L, Schleper C (2008) Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol 64:167–174

    Article  CAS  PubMed  Google Scholar 

  • Reunov AA, Au DWT, Wu RSS (1999) Spermatogenesis of the green-lipped mussel Perna viridis with dual patterns of acrosome and tail development in spermatids. Helgol Mar Res 53:62–69

    Article  Google Scholar 

  • Schouten S, Villanueva L, Hopmans EC, van der Meer MT, Sinninghe Damsté JS (2014) Are marine group II Euryarchaeota significant contributors to tetraether lipids in the ocean? Proc Natl Acad Sci USA 111:E4285. doi:10.1073/pnas.1416176111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sela-Adler M, Said-Ahmad W, Sivan O, Eckert W, Kiene RP, Amrani A (2016) Isotopic evidence for the origin of dimethylsulfide and dimethylsulfoniopropionate-like compounds in a warm, monomictic freshwater lake. Environ Chem 13:340–351

    Article  CAS  Google Scholar 

  • Shaw GE (1983) Bio-controlled thermostasis involving the sulfur cycle. Clim Change 5:297–303

    Article  CAS  Google Scholar 

  • Siboni N, Ben-Dov E, Sivan A, Kushmaro A (2008) Global distribution and diversity of coral-associated Archaea and their possible role in the coral holobiont nitrogen cycle. Environ Microbiol 10:2979–2990

    Article  CAS  PubMed  Google Scholar 

  • Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR et al (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103:12115–12120. doi:10.1073/pnas.0605127103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terranova MS, Lo Brutto S, Arculeo M, Mitton JB (2006) Population structure of Brachidontes pharaonis (P. Fisher, 1870) (Bivalvia, Mytilidae) in the Mediterranean Sea, and evolution of a novel mtDNA polymorphism. Mar Biol 150:89–101

    Article  Google Scholar 

  • Tomascik T, Mah AJ (1994) The ecology of ‘Halimeda lagoon”: an anchialine lagoon of a raised atoll, Kakaban island, East Kalimantan, Indonesia. Tropical Biodivers 2:385–399

    Google Scholar 

  • Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A, Urich T et al (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci USA 108:8420–8425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turich C, Freeman KH, Bruns MA, Conte M, Jones AD, Wakeham SG (2007) Lipids of marine Archaea: patterns and provenance in the water-column and sediments. Geochim Cosmochim Acta 71:3272–3291

    Article  CAS  Google Scholar 

  • Urcuyo IA, Massoth GJ, Julian D, Fishe CR (2003) Habitat, growth and physiological ecology of a basaltic community of Ridgeia piscesae from the Juan de Fuca Ridge. Deep Sea Research Part I 50:763–780

    Article  CAS  Google Scholar 

  • van Hoek AH, van Alen TA, Sprakel VS, Leunissen JA, Brigge T, Vogels GD, Hackstein JH (2000) Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates. Mol Biol Evol 17:251–258

    Article  PubMed  Google Scholar 

  • Vaz-Moreira I, Egas C, Nunes OC, Manaia CM (2011) Culture-dependent and culture-independent diversity surveys target different bacteria: a case study in a freshwater sample. A Van Leeuw J Microb 100:245–257

    Article  Google Scholar 

  • Visscher PT, Guidetti JR, Culbertson CW, Oremland RS (1996) Dimethylsulfoniopropionate as a potential methanogenic substrate in Mono Lake sediments. In: biological and environmental chemistry of DMSP and related sulfonium compounds. Springer, US, pp 361–368

  • Wagner C, Stadtman ER (1962) Bacterial fermentation of dimethyl-β-propiothetin. Arch Biochem Biophys 98:331–336

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 73:5261–5267

    Article  CAS  Google Scholar 

  • Wang JX, Zhang CL, Xie W, Zhang YG, Wang P (2015) Contribution of Marine Group II Euryarchaeota to cyclopentyl tetraethers in the Pearl River estuary and coastal South China Sea: impact on the TEX86 paleothermometer. Biogeosci Discus 12:12455–12484

    Article  Google Scholar 

  • Webster NS, Negri AP, Munro MM, Battershill CN (2004) Diverse microbial communities inhabit Antarctic sponges. Environ Microbiol 6:288–300

    Article  PubMed  Google Scholar 

  • Winters AD, Marsh TL, Faisal M (2011) Heterogeneity of bacterial communities within the zebra mussel (Dreissena polymorpha) in the Laurentian Great Lakes Basin. J Great Lakes Res 37:318–324

    Article  Google Scholar 

  • Wuchter C, Abbas B, Coolen MJ, Herfort L, van Bleijswijk J, Timmers P (2006) Archaeal nitrification in the ocean. Proc Natl Acad Sci USA 103:12317–12322. doi:10.1073/pnas.0600756103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong J, Dai W, Zhu J, Liu K, Dong C, Qiu Q (2017) The underlying ecological processes of Gut Microbiota among Cohabitating retarded, overgrown and normal Shrimp. Microb Ecol 73:988–999

    Article  PubMed  Google Scholar 

  • Yau S, Lauro FM, Williams TJ, DeMaere MZ, Brown MV, Rich J et al (2013) Metagenomic insights into strategies of carbon conservation and unusual sulfur biogeochemistry in a hypersaline Antarctic lake. ISME J 7:1944–1961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeager MM, Cherry DS, Neves RJ (1994) Feeding and burrowing behaviors of juvenile rainbow mussels, Villosa iris (Bivalvia: Unionidae). J N Am Benthol Soc 13:217–222

    Article  Google Scholar 

  • Yoch DC (2002) Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide. Appl Environ Microb 68:5804–5815

    Article  CAS  Google Scholar 

  • Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89:670–679

    Article  CAS  PubMed  Google Scholar 

  • Zhang CL, Xie W, Martin-Cuadrado AB, Rodriguez-Valera F (2015) Marine Group II Archaea, potentially important players in the global ocean carbon cycle. Front Microbiol 6:1108

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The research was sponsored by the Indonesian Institute of Sciences (LIPI) and the Portuguese Foundation for Science and Technology, FCT, project LESS CORAL, PTDC/AAC-AMB/115304/2009. We are grateful to the Indonesian State Ministry of Research and Technology (RISTEK) for providing research permits. We thank the following people for their help in various ways: LE Becking, Y. Tuti, N. de Voogd, E. Oberhauser, R. Suhr, and the staff of Nabucco Island Dive Resort.

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  1. CESAM and Department of Biology, Universidade de Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal

    D. F. R. Cleary & A. R. M. Polónia

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  1. D. F. R. Cleary
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  2. A. R. M. Polónia
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Correspondence to D. F. R. Cleary.

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Cleary, D.F.R., Polónia, A.R.M. Bacterial and archaeal communities inhabiting mussels, sediment and water in Indonesian anchialine lakes. Antonie van Leeuwenhoek 111, 237–257 (2018). https://doi.org/10.1007/s10482-017-0944-1

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  • DOI: https://doi.org/10.1007/s10482-017-0944-1

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