Abstract
The Hawaiian Archipelago is a “biodiversity hotspot” where significant endemism among eukaryotes has evolved through geographic isolation and local topography. To address the absence of corresponding region-wide data on Hawaii’s microbiota, we compiled the first 16S SSU rDNA clone libraries and cultivated bacteria from five Hawaiian lakes, an anchialine pool, and the Lō’ihi submarine volcano. These sites offer diverse niches over ~5000 m elevation and ~1150 nautical miles. Each site hosted a distinct prokaryotic community dominated by Bacteria. Cloned sequences fell into 158 groups from 18 Bacteria phyla, while seven were unassigned and two belonged in the Euryarchaeota. Only seven operational taxonomic units (each OTU comprised sequences that shared ≥97% sequence identity) occurred in more than one site. Pure bacterial cultures from all sites fell into 155 groups (each group comprised pure cultures that shared ≥97% 16S SSU rDNA sequence identity) from 10 Bacteria phyla; 15 Proteobacteria and Firmicutes were cultivated from more than one site. One hundred OTUs (60%) and 52 (33.3%) cultures shared <97% 16S SSU rDNA sequence identity with published sequences. Community structure reflected habitat chemistry; most δ-Proteobacteria occurred in anoxic and sulfidic waters of one lake, while β-Proteobacteria were cultivated exclusively from fresh or brackish waters. Novel sequences that affiliate with an Antarctic-specific clade of Deinococci, and Candidate Divisions TM7 and BRC1, extend the geographic ranges of these phyla. Globally and locally remote, as well as physically and chemically diverse, Hawaiian aquatic habitats provide unique niches for the evolution of novel communities and microorganisms.
Similar content being viewed by others
References
MA Allen (1959) ArticleTitleStudies with Cyanidium caldarium, an anomalously pigmented chlorophyte. Arch Microbiol 32 270–277 Occurrence Handle1:STN:280:CyaD2MjmvVI%3D
SF Altschul TL Madden AA Schäffer J Zhang Z Zhang W Miller DJ Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389–3402 Occurrence Handle1:CAS:528:DyaK2sXlvFyhu7w%3D Occurrence Handle9254694
RM Atlas LC Parks (1996) Handbook of Microbiological Media, 2nd ed. CRC Press Boca Raton, FL, p 166
SM Barns RE Fundyga MW Jeffries NR Pace (1994) ArticleTitleRemarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc Natl Acad Sci USA 91 1609–1613 Occurrence Handle1:CAS:528:DyaK2cXitFanurw%3D Occurrence Handle7510403
J Bell J Betts E Boyle (2002) ArticleTitleMITESS: a moored in situ trace element serial sampler for deep-sea moorings. Deep-Sea Res I 49 2103–2118 Occurrence Handle10.1016/S0967-0637(02)00126-7 Occurrence Handle1:CAS:528:DC%2BD38XpsFWhu7Y%3D
GDR Carr RH Robichaux MS Witter DW Kyhos (1989) Adaptive radiation of the Hawaiian silversword alliance (Compositae-Madiinae): a comparison with Hawaiian picture-winged Drosophila. LVS Giddings KY Kaneshiro WW Anderson (Eds) Genetics, Speciation and the Founder Principle Oxford University Press New York 79–97
RW Castenholz (1981) Isolation and cultivation of thermophilic cyanobacteria. MP Starr H Stolp HG Trüper A Balows HG Schlegel (Eds) The Prokaryotes, Vol. 1 Springer-Verlag Berlin 236–246
JR Cole BB Chai TL Marsh RJ Farris Q Wang SA Kulam S Chandra DM McGarrell TM Schmidt GM Garrity JM Tiedje (2003) ArticleTitleThe Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31 442–443 Occurrence Handle10.1093/nar/gkg039 Occurrence Handle1:CAS:528:DC%2BD3sXhvFSls7o%3D Occurrence Handle12520046
TP Curtis WT Sloan JW Scannell (2002) ArticleTitleEstimating prokaryotic diversity and its limits. Proc Natl Acad Sci USA 99 10494–10499
JR de la Torre BM Goebel EI Friedmann NR Pace (2003) ArticleTitleMicrobial diversity of cryptoendolithic communities from the McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 69 3858–3867 Occurrence Handle10.1128/AEM.69.7.3858-3867.2003 Occurrence Handle1:CAS:528:DC%2BD3sXlsFagt74%3D Occurrence Handle12839754
M Derakshani T Lukow W Liesack (2001) ArticleTitleNovel bacterial lineages at the (sub)division level as detected by signature nucleotide-targeted recovery of 16S rRNA genes from bulk soil and rice roots of flooded rice microcosms. Appl Environ Microbiol 67 623–631 Occurrence Handle10.1128/AEM.67.2.623-631.2001 Occurrence Handle1:CAS:528:DC%2BD3MXhtFSmuro%3D Occurrence Handle11157225
SP Donachie JP Bowman M Alam (2004) ArticleTitlePsychroflexus tropicus, sp. nov., a novel, obligately halophilic Cytophaga-Flavobacterium-Bacteroides group bacterium isolated from an Hawaiian hypersaline lake. Int J Syst Evol Microbiol 54 935–940 Occurrence Handle10.1099/ijs.0.02733-0 Occurrence Handle1:CAS:528:DC%2BD2cXlt1emt7k%3D Occurrence Handle15143045
SP Donachie BW Christenson DD Kunkel A Malahoff M Alam (2002) ArticleTitleMicrobial community in acidic hydrothermal waters of volcanically active White Island, New Zealand. Extremophiles 6 419–425 Occurrence Handle10.1007/s00792-002-0274-7 Occurrence Handle1:CAS:528:DC%2BD38XnvVCisbc%3D Occurrence Handle12382119
SP Donachie TS Gregory S Hou A Malahoff M Alam (2003) ArticleTitleIdiomarina loihiensis, sp. nov., a novel, halophilic γ-Proteobacterium from the Lō’ihi submarine volcano, Hawai’i. Int J Syst Evol Microbiol 53 1873–1879 Occurrence Handle10.1099/ijs.0.02701-0 Occurrence Handle1:CAS:528:DC%2BD2cXhtF2hsA%3D%3D Occurrence Handle14657116
SP Donachie RA Kinzie III RR Bidigare DW Sadler DM Karl (1999) ArticleTitleLake Kauhakō, Moloka’i, Hawai’i: biological and chemical aspects of a morpho-ectogenic meromictic lake. Aquat Microb Ecol 19 93–103
SP Donachie R Saborowski G Peters F Buchholz (1995) ArticleTitleBacterial digestive enzyme activity in the stomach and hepatopancreas of Meganyctiphanes norvegica (M. Sars, 1857). J Exp Mar Biol Ecol 188 151–165
SP Donachie MK Zdanowski (1998) ArticleTitlePotential digestive function of bacteria in krill, Euphausia superba stomach. Aquat Microb Ecol 14 129–136
JE Dore R Lukas DW Sadler DM Karl (2003) ArticleTitleClimate-driven changes to the atmospheric CO2 sink in the subtropical North Pacific Ocean. Nature 424 754–757 Occurrence Handle10.1038/nature01885 Occurrence Handle1:CAS:528:DC%2BD3sXmt1ant78%3D Occurrence Handle12917678
N Dubilier C Mulders T Ferdelman D De Beer A Pernthaler M Klein M Wagner C Erseus F Thiermann J Krieger O Giere R Amann (2001) ArticleTitleEndosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm. Nature 411 298–302 Occurrence Handle10.1038/35077067 Occurrence Handle1:STN:280:DC%2BD3M3msVygtQ%3D%3D Occurrence Handle11357130
KJ Edwards DR Rogers CO Wirsen TM McCollom (2003) ArticleTitleIsolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic α- and γ-Proteobacteria from the deep sea. Appl Environ Microbiol 69 2906–2913 Occurrence Handle10.1128/AEM.69.5.2906-2913.2003 Occurrence Handle1:CAS:528:DC%2BD3sXjslOlt7w%3D Occurrence Handle12732565
B Eichler N Pfennig (1988) ArticleTitleA new purple sulfur bacterium from stratified freshwater lakes, Amoebobacter purpureus sp. nov. Arch Microbiol 149 395–400 Occurrence Handle1:CAS:528:DyaL1cXhvVemtLw%3D
H Eilers J Pernthaler FO Glöckner R Amann (2000) ArticleTitleCulturability and in situ abundance of pelagic bacteria from the North Sea. Appl Environ Microbiol 66 3044–3051 Occurrence Handle10.1128/AEM.66.7.3044-3051.2000 Occurrence Handle1:CAS:528:DC%2BD3cXkslKlt7k%3D Occurrence Handle10877804
D Emerson CL Moyer (2002) ArticleTitleNeutrophilic Fe-oxidizing bacteria are abundant at the Loihi Seamount hydrothermal vents and play a major role in Fe oxide deposition. Appl Environ Microbiol 68 3085–3093 Occurrence Handle10.1128/AEM.68.6.3085-3093.2002 Occurrence Handle1:CAS:528:DC%2BD38XksVWqtLw%3D Occurrence Handle12039770
CA Francis BM Tebo (2002) ArticleTitleEnzymatic manganese(II) oxidation by metabolically dormant spores of diverse Bacillus species. Appl Environ Microbiol 68 874–880 Occurrence Handle10.1128/AEM.68.2.874-880.2002 Occurrence Handle1:CAS:528:DC%2BD38XhtV2nsbw%3D Occurrence Handle11823231
TE Freitag JI Prosser (2003) ArticleTitleCommunity structure of ammonia-oxidizing bacteria within anoxic marine sediments. Appl Environ Microbiol 69 1359–1371 Occurrence Handle10.1128/AEM.69.3.1359-1371.2003 Occurrence Handle1:CAS:528:DC%2BD3sXitlCmu7w%3D Occurrence Handle12620817
SJ Giovannoni MS Rappé (2000) Evolution, diversity, and molecular ecology of marine prokaryotes. DL Kirchman (Eds) Microbial Ecology of the Ocean Wiley Interscience New York 47–84
FO Glöckner BM Fuchs R Amann (1999) ArticleTitleBacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65 3721–3726 Occurrence Handle10427073
JM González RP Kiene MA Moran (1999) ArticleTitleTransformation of sulfur compounds by an abundant lineage of marine bacteria in the α-subclass of the class Proteobacteria. Appl Environ Microbiol 65 3810–3819 Occurrence Handle10473380
Gros, O, Liberge, M, Felbeck, HA (2003) Detection of the free-living form of sulphide-oxidizing gill endosymbionts in the environment: case study of Codakia orbicularis. Abstract, ASLO 2003 Aquatic Sciences Meeting, Salt Lake City, UT
Å Hagström T Pommier F Rohwer K Simu W Stolte D Svensson UL Zweifel (2002) ArticleTitleUse of 16S ribosomal DNA for delineation of marine bacterioplankton species. Appl Environ Microbiol 68 3628–3633 Occurrence Handle10.1128/AEM.68.7.3628-3633.2002 Occurrence Handle12089052
Y Hongoh H Yuzawa M Ohkuma T Kudo (2003) ArticleTitleEvaluation of primers and PCR conditions for the analysis of 16S rRNA genes from a natural environment. FEMS Microbiol Lett 221 299–304 Occurrence Handle10.1016/S0378-1097(03)00218-0 Occurrence Handle1:CAS:528:DC%2BD3sXjtlSlu7c%3D Occurrence Handle12725942
DM Karl AM Brittain BD Tilbrook (1989) ArticleTitleHydrothermal and microbial processes at Loihi Seamount, a mid-plate hot-spot volcano. Deep-Sea Res 36 1655–1673 Occurrence Handle10.1016/0198-0149(89)90065-4 Occurrence Handle1:CAS:528:DyaK3MXpvVag
M Kimura (1983) The neutral theory of molecular evolution. M Nei R Koehn (Eds) Evolution of Genes and Proteins Sinauer Associates Sunderland, MA 208–233
GM King (2003) ArticleTitleContributions of atmospheric CO and hydrogen uptake to microbial dynamics on recent Hawaiian volcanic deposits. Appl Environ Microbiol 69 4067–4075 Occurrence Handle10.1128/AEM.69.7.4067-4075.2003 Occurrence Handle1:CAS:528:DC%2BD3sXlsFagtbc%3D Occurrence Handle12839783
S Kumazawa A Mitsui (1981) ArticleTitleCharacterization and optimization of hydrogen photoproduction by a saltwater blue-green alga, Oscillatoria sp. Miami BG7. I Enhancement through limiting the supply of nitrogen nutrients. Int J Hydrogen Energy 6 341–350
N Kurosawa YH Itoh T Iwai A Sugai I Uda N Kimura T Horiuchi T Itoh (1998) ArticleTitleSulfurisphaera ohwakuensis gen. nov., sp. nov., a novel extremely thermophilic acidophile of the order Sulfolobales. Int J Syst Bacteriol 48 451–456 Occurrence Handle9731283
DJ Kushner (1992) Growth and nutrition of halophilic bacteria. RH Vreeland LI Hochstein (Eds) The Biology of Halophilic Bacteria CRC Press Boca Raton, FL 87–104
DJ Lane (1991) 16S/23S rRNA sequencing. E Stackebrandt M Goodfellow (Eds) Nucleic Acid Techniques in Bacterial Systematics John Wiley and Sons New York 115–175
EA Laws AH Woodcock (1981) ArticleTitleHypereutrophication of an Hawaiian Alpine Lake. Pac Sci 35 257–261 Occurrence Handle1:CAS:528:DyaL38XhsVylurY%3D
JR Leadbetter (2003) ArticleTitleCultivation of recalcitrant microbes: cells are alive, well and revealing their secrets in the 21st century laboratory. Curr Opin Microbiol 6 274–281 Occurrence Handle10.1016/S1369-5274(03)00041-9 Occurrence Handle1:CAS:528:DC%2BD3sXkvVKgu74%3D Occurrence Handle12831904
A Maciolek (1982) ArticleTitleLakes and lake-like waters of the Hawaiian Archipelago. Occ Pap Bernice P Bishop Mus 25 1–14
A Malahoff TS Gregory A Bossuyt SP Donachie M Alam (2002) ArticleTitleA seamless system for the collection and cultivation of extremophiles from deep-ocean hydrothermal vents. IEEE J Ocean Eng 27 862–868 Occurrence Handle10.1109/JOE.2002.804058
J Marmur (1961) ArticleTitleA procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 3 208–218 Occurrence Handle1:CAS:528:DyaF3MXosl2kuw%3D%3D
J Miyake X-Y Mao S Kawamura (1984) ArticleTitlePhotoproduction of hydrogen from glucose by a co-culture of a photosynthetic bacterium and Clostridium butyricum. J Ferment Technol 62 531–535 Occurrence Handle1:CAS:528:DyaL2MXnslajsg%3D%3D
CL Moyer FC Dobbs DM Karl (1994) ArticleTitleEstimation of diversity and community structure through restriction fragment length polymorphism distribution analysis of bacterial 16S rRNA genes from a microbial mat at an active, hydrothermal vent system, Loihi Seamount, Hawaii. Appl Environ Microbiol 60 871–879 Occurrence Handle1:CAS:528:DyaK2cXivFSqs74%3D Occurrence Handle7512808
CL Moyer FC Dobbs DM Karl (1995) ArticleTitlePhylogenetic diversity of the bacterial community from a microbial mat at an active, hydrothermal vent system, Loihi Seamount, Hawaii. Appl Environ Microbiol 61 1555–1562 Occurrence Handle1:CAS:528:DyaK2MXksl2ltrw%3D Occurrence Handle7538279
MA Munson T Pitt-Ford B Chong A Weightman WG Wade (2002) ArticleTitleMolecular and cultural analysis of the microflora associated with endodontic infections. J Dent Res 81 761–766 Occurrence Handle1:CAS:528:DC%2BD38XovFKmsrg%3D Occurrence Handle12407091
N Myers RA Mittermeier CG Mittermeier GAB da Fonseca J Kent (2000) ArticleTitleBiodiversity hotspots for conservation priorities. Nature 403 853–858 Occurrence Handle10.1038/35002501 Occurrence Handle1:CAS:528:DC%2BD3cXhs1Olsr4%3D Occurrence Handle10706275
K Nüsslein JM Tiedje (1998) ArticleTitleCharacterization of the dominant and rare members of a young Hawaiian soil bacterial community with small-subunit ribosomal DNA amplified from DNA fractionated on the basis of its guanine and cytosine composition. Appl Environ Microbiol 64 1283–1289
RDM Page (1996) ArticleTitleAn application to display phylogenetic trees on personal computers. Comp Applic Biol Sci 12 357–358
MF Polz CM Cavanaugh (1998) ArticleTitleBias in template-to-product ratios in multitemplate PCR. Appl Environ Microbiol 64 3724–3730 Occurrence Handle1:CAS:528:DyaK1cXms1entrc%3D Occurrence Handle9758791
AL Reysenbach K Longnecker J Kirshtein (2000) ArticleTitleNovel bacterial and archaeal lineages from an in situ growth chamber deployed at a Mid-Atlantic Ridge hydrothermal vent. Appl Environ Microbiol 66 3798–3806 Occurrence Handle10.1128/AEM.66.9.3798-3806.2000 Occurrence Handle1:CAS:528:DC%2BD3cXmsVWqu7k%3D Occurrence Handle10966393
Sedwick, PN (1991) Chemistry of hydrothermal solutions from Pele’s Vents, Loihi Seamount, Hawaii. PhD thesis, University of Hawaii, p 154
E Stackebrandt BM Goebel (1994) ArticleTitleTaxonomic note: A place for DNA:DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44 846–849 Occurrence Handle1:CAS:528:DyaK2MXitFCnsb4%3D
RY Stanier NJ Palleroni M Doudoroff (1966) ArticleTitleThe aerobic pseudomonads: a taxonomic study. J Gen Microbiol 43 159–271 Occurrence Handle1:STN:280:CCiC38fhtlU%3D Occurrence Handle5963505
Strickland, JDH, Parsons, TR (1972) A Practical Handbook of Seawater Analysis. Fisheries Research Board of Canada
M Strous JA Fuerst EHM Kramer S Logemann G Muyzer KT van de Pas Schoonen R Webb JG Kuenen MS Jetten (1999) ArticleTitleMissing lithotroph identified as new planctomycete. Nature 400 446–449 Occurrence Handle10.1038/22749 Occurrence Handle1:CAS:528:DyaK1MXltVGnt7c%3D Occurrence Handle10440372
MT Suzuki SJ Giovannoni (1996) ArticleTitleBias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl Environ Microbiol 62 625–630 Occurrence Handle1:CAS:528:DyaK28XovVCrug%3D%3D Occurrence Handle8593063
A Teske T Brinkhoff G Muyzer DP Moser J Rethmeier HW Jannasch (2000) ArticleTitleDiversity of thiosulfate-oxidizing bacteria from marine sediments and hydrothermal vents. Appl Environ Microbiol 66 3125–3133 Occurrence Handle10.1128/AEM.66.8.3125-3133.2000 Occurrence Handle1:CAS:528:DC%2BD3cXlsFaktbo%3D Occurrence Handle10919760
JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe CLUSTALX Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24 4876–4882 Occurrence Handle10.1093/nar/25.24.4876
C Vetriani HW Jannasch BJ MacGregor DA Stahl AL Reysenbach (1999) ArticleTitlePopulation structure and phylogenetic characterization of marine benthic Archaea in deep-sea sediments. Appl Environ Microbiol 65 4375–4384 Occurrence Handle1:CAS:528:DyaK1MXms1Ois7c%3D Occurrence Handle10508063
Acknowledgments
This work was supported under NSF Microbial Observatories Program grant no. MCB0084326 to MA. We thank the US Fish and Wildlife Service and the Department of Land and Natural Resources for assistance during planning for sample collection. We are indebted to Dr. Jim Maragos, Chief Scientist of the NOW-RAMP-II cruise, for his support during the cruise. Thanks also to Dr. Dave Gulko and the captain and crew of the MV Rapture, plus the NOW-RAMP II participants; to the captain and crew of the RV Ka’imikai-o-kanaloa, and the DSRV Pisces V pilot Terry Kerby and team; Ron Nagata (Chief, Division of Resources Management, Haleakela National Park, National Park Service), field guide Terry Lind (HNP), and helicopter pilot Richard ‘Duke’ Baldwin, Maui; William Appleton and Randolph McCreight for access to Green Lake; NPS Kalaupapa Superintendents Guy Hughes, Bill Eichenlaub, Dean Alexander, and Ranger Jeff Trainer assisted at L. Kauhakō. Field assistance was provided by Ritchie Araneta, Renee Harada, Horst-Volker Henschel, Brian Neville, Jimmy Saw, Mandelle Ruiz, Mark Speck, and Lance Tamashiro. Jeanette Fu, Kalle Johansson, Minh Hinh Nguyen, Abigail Perucho-Gicewicz, and Li Zhou assisted in the laboratory. Thanks to Dr. JoAnn Radway for advice and assistance with cyanobacteria isolations.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Donachie, S., Hou, S., Lee, K. et al. The Hawaiian Archipelago: A Microbial Diversity Hotspot. Microb Ecol 48, 509–520 (2004). https://doi.org/10.1007/s00248-004-0217-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-004-0217-1