Wind and sunlight shape microbial diversity in surface waters of the North Pacific Subtropical Gyre

ISME Journal

Volumn 10, Issue 6, 2016, Pages 1308-1322

  Bryant, Jessica A ^a,b   Aylward, Frank O ^b   Eppley, John M ^b   Karl, David M ^b   Church, Matthew J ^b   DeLong, Edward F ^a,b  

^a Massachusetts Institute of Technology   (United States)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; COEXISTENCE; COMMUNITY COMPOSITION; ENVIRONMENTAL FACTOR; GENE; GENETIC ANALYSIS; GENOMICS; GYRE; LIGHT EFFECT; MICROBIAL COMMUNITY; SEASONAL VARIATION; SEASONALITY; SOLAR RADIATION; SURFACE WATER; WIND VELOCITY;

ALOHA STATION; PACIFIC OCEAN; PACIFIC OCEAN (NORTH);

BACTERIA (MICROORGANISMS);

SEA WATER;

BIODIVERSITY; ECOSYSTEM; HAWAII; METAGENOMICS; MICROBIAL CONSORTIUM; MICROBIOLOGY; PACIFIC OCEAN; PHYLOGENY; PLANKTON; SEASON; SUNLIGHT; WIND;

BIODIVERSITY; ECOSYSTEM; HAWAII; METAGENOMICS; MICROBIAL CONSORTIA; PACIFIC OCEAN; PHYLOGENY; PLANKTON; SEASONS; SEAWATER; SUNLIGHT; WIND;

EID: 84949257419     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.221     Document Type: Article

References (96)

1. Allen B, Kon M, Bar-Yam Y. (2009). A new phylogenetic diversity measure generalizing the Shannon index and its application phyllostomid bats. Am Nat 174: 236-243
2. An-Yi T, Chin W-M, Chiang K-P. (2009). Diel patterns of grazing by pigmented nanoflagellates on Synechococcus spp. in the coastal ecosystem of subtropical western Pacific. Hydrobiologia 636: 249-256
3. Aylward FO, Eppley JM, Smith JM, Chavez FP, Scholin CA, DeLong EF. (2015).Microbial community transcriptional networks are conserved in three domains at the ocean basin scales. Proc Natl Acad Sci USA 17: 5443-5448
4. Barberán A, Fernández-Guerra A, Bohannan BJM, Casamayor EO. (2012). Exploration of community traits as ecological markers in microbial metagenomics. Mol Ecol 8: 1909-1917
5. Bidigare RR, Chai F, Landry MR, Lukas R, Hannides CCS, Christensen SJ, et al. (2009). Subtropical ocean ecosystem structure changes forced by North Pacific climate variations. J Plankton Res 31: 1131-1139
6. Bingham FM, Lukas R. (1996). Seasonal cycles of temperature, salinity and dissolved oxygen observed in the Hawaii Ocean Time-series. Deep Sea Res Part 2 Top Stud Oceanogr 43: 199-213
7. Brown MV, Philip GK, Bunge JA, Smith MC, Bissett A, Lauro FM, et al. (2009). Microbial community structure in the North Pacific ocean. ISME J 3: 1374-1386
8. Bryant JA, Stewart FJ, Eppley JM, DeLong EF. (2012). Microbial community phylogenetic and trait diversity declines with depth in a marine oxygen minimum zone. Ecology 93: 1659-1673
9. Campbell L, Vaulot D. (1993). Photosynthetic picoplankton community structure in the subtropical North Pacific Ocean near Hawaii (Station ALOHA). Deep Sea Res Part 1 Oceanogr Res Pap 40: 2043-2060
10. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. (2010). PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26: 266-267
11. 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
12. Carlson CA, Morris R, Parsons R, Treusch AH, Giovannoni SJ, Vergin K. (2009). Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea. ISMEJ 3: 283-295
13. Crescenti GH, Payne RE, Weller RA. (1989). Improved meteorological measurements from buoys and ships (IMET): preliminary comparison of pyranometers. WHOI Tech Reports. WHOI-89-47, IMETTR-89-04. Woods Hole Oceanographic Institution: Woods Hole, MA, USA
14. Csardi G, Nepusz T. (2006). The igraph software package for complex network research. InterJournal Complex Systems, 1695
15. DeLong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard N-U, et al. (2006). Community genomics among stratified microbial assemblages in the oceans interior. Science 311: 496-503
16. DiTullio GR, Laws EA. (1991). Impact of an atmosphericoceanic disturbance on phytoplankton community dynamics in the North Pacific Central Gyre. Deep Sea Res A 38: 1305-1329
17. DuRand MD, Olson RJ, Chisholm SW. (2001). Phytoplankton population dynamics at the Bermuda Atlantic Time-series station in the Sargasso Sea. Deep Sea Res Part 2 Top Stud Oceanogr 48: 1983-2003
18. Edgar RC. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461
19. Eiler A, Hayakawa DH, Rappé MS. (2011). Non-random assembly of bacterioplankton communities in the subtropical North Pacific Ocean. Front Microbiol 2: 140
20. Faith DP. (1992). Conservation evaluation and phylogenetic diversity. Biol Conserv 61: 1-10
21. Fierer N, Leff J, Adams B, Nielsen UN, Bates ST, Lauber CL, et al. (2012). Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Natl Acad Sci USA 109: 21390-21395
22. Fitzsimmons JN, Hayes CT, Al-Subiai SN, Zhang R, Morton PL, Weisend RE, et al. (2015). Daily to decadal variability of size-fractionated iron and iron-binding ligand at the Hawaii Ocean Time-series Station ALOHA. Geochim Cosmochim Acta 171: 303-324
23. Fong AA, Karl DM, Lukas R, Letelier RM, Zehr JP, Church MJ. (2008). Nitrogen fixation in an anticyclonic eddy in the oligotrophic North Pacific Ocean. ISME J 2: 663-676
24. Frith MC, Hamada M, Horton P. (2010). Parameters for accurate genome alignment. BMC Bioinformatics 11: 80
25. Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV, Naeem S. (2006). Annually reoccurring bacterial communities are predictable from ocean conditions. Proc Natl Acad Sci USA 103: 13104-13109
26. Ghiglione J-F, Galand PE, Pommier T, Pedrós-Alió C, Maas EW, Bakker K, et al. (2012). Pole-To-pole biogeography of surface and deep marine bacterial communities. Proc Natl Acad Sci USA 109: 17633-17638
27. Gilbert JA, Field D, Swift P, Thomas S, Cummings D, Temperton B, et al. (2010). The taxonomic and functional diversity of microbes at a temperate coastal site: a multi-omic study of seasonal and diel temporal variation. PLoS One 5: e15545
28. Gilbert JA, Steele JA, Caporaso JG, Steinbrück L, Reeder J, Temperton B, et al. (2012). Defining seasonal marine microbial community dynamics. ISME J 6: 298-308
29. Giovannoni SJ, Rappe MS, Vergin KL, Adair NL. (1996). 16S rRNA genes reveal stratified open ocean bacterioplankton populations related to the Green Non-Sulfur bacteria. Proc Natl Acad Sci USA 93: 7979-7984
30. Giovannoni SJ, Vergin KL. (2012). Seasonality in ocean microbial communities. Science 335: 671-676
31. Gordon D, Giovannoni S. (1996). Detection of stratified microbial populations related to Chlorobium and Fibrobacter species in the Atlantic and Pacific oceans. Appl Environ Microbiol 62: 1171-1177
32. Hansman RL, Griffin S, Watson JT, Druffel ERM, Ingalls AE, Pearson A, et al. (2009). The radiocarbon signature of microorganisms in the mesopelagic ocean. Proc Natl Acad Sci USA 106: 6513-6518
33. Ingalls AE, Shah SR, Hansman RL, Aluwihare LI, Santos GM, Druffel ERM, et al. (2006). Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc Natl Acad Sci USA 103: 6442-6447
34. Jickells TD, An ZS, Andersen KK, Baker a R, Bergametti G, Brooks N, et al. (2005). Global iron connections between desert dust, ocean, biogeochemistry and climate. Science 308: 67-71
35. Jing H, Xia X, Suzuki K, Liu H. (2013). Vertical profiles of bacteria in the tropical and subarctic oceans revealed by pyrosequencing. PLoS One 8: e79423
36. Johnson ZI, Zinser ER, Coe A, McNulty NP, Woodward EMS, Chisholm SW. (2006). Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311: 1737-1740
37. Jones E, Oliphant T, Peterson P, Others A. (2001), SciPy: Open source scientific tools for python. Available at: http://www.scripy.org/ (accesse 15 September 2013
38. Jumpstart Consortium Human Microbiome Project Data Generation Working Group. (2012). Evaluation of 16S rDNA-based community profiling for human microbiome research. PLoS One 7: e39315
39. Kahru M, Gille ST, Murtugudde R, Strutton PG, Manzano-Sarabia M, Wang H, Mitchell BG. (2010). Global correlations between winds and ocean chlorophyll. J Geophys Res 115: C12040
40. Kanehisa M, Goto S. (2000). KEGG: Kyoto encyclopedia of genomes and genomes. Nucl Acids Res 28: 27-30
41. Karl DM, Church MJ, Dore JE, Letelier RM, Mahaffey C. (2012). Predictable and efficient carbon sequestration in the North Pacific Ocean supported by symbiotic nitrogen fixation. Proc Natl Acad Sci USA 109: 1842-1849
42. Karl DM, Church MJ. (2014). Microbial oceanography and the Hawaii Ocean Time-series programme. Nature Rev Micro 12: 699-713
43. Karl DM, Knauer GA, Martin JH, Ward BB. (1984). Bacterial chemolithotrophy in the ocean is associated with sinking particles. Nature 309: 54-56
44. Karl DM, Lukas R. (1996). The Hawaii Ocean Time-series (HOT) program: Background, rationale and field implementation. Deep-Sea Res Part 2 Top Stud Oceanogr 43: 129-156
45. Karl DM, Tien G. (1997). Temporal variability in dissolved phosphorus concentrations in the subtropical North Pacific Ocean. Mar Chem 56: 77-96
46. Kashtan N, Roggensack SE, Rodrigue S, Thompson JW, Biller SJ, Coe A, et al. (2014). Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science 344: 416-420
47. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, et al. (2010). Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26: 1463-1464
48. Kembel SW, Eisen JA, Pollard KS, Green JL. (2011). The phylogenetic diversity of metagenomes. PLoS One 6: e23214
49. Kettler GC, Martiny AC, Huang K, Zucker J, Coleman ML, Rodrigue S, et al. (2007). Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet 3: 2515-2528
50. Ladau J, Sharpton TJ, Finucane MM, Jospin G, Kembel SW, ODwyer J, et al. (2013). Global marine bacterial diversity peaks at high latitudes in winter. ISMEJ 7: 1669-1677
51. Langfelder P, Horvath S. (2008). WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9: 559
52. Lechner M, Findeib S, Steiner L, Marz M, Stadler PF, Prohaska SJ. (2011). Proteinortho: detection of (Co-)orthologs in large-scale analysis. BMC Bioinformatics 12: 124
53. Lee S, Fuhrman JA. (1991). Spatial and temporal variation of natural bacterioplankton assemblages studied by total genomic DNA cross-hybridization. Limnol Oceanogr 36: 1277-1287
54. Letelier R, Karl DM, Abbott MR, Flament P, Freilich M, Lukas R, et al. (2000). Role of late winter mesoscale events in the biogeochemical variability of the upper water column of the North Pacific Subtropical Gyre. J Geophys Res 105: 28723-28739
55. Letelier RM, Bidigare RR, Hebel DV, Ondrusek M, Winn CD, Karl DM. (1993). Temporal variability of phytoplankton community structure based on pigment analysis. Limnol Oceanogr 38: 1420-1437
56. Li W, Godzik A. (2006). Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659
57. Logares R, Sunagawa S, Salazar G, Cornejo-Castillo FM, Ferrera I, Sarmenta H, Hingamp P, et al. (2009). Metagenomic 16S rDNA Illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities. Environ Microbiol 16: 2659-2671
58. Love MI, Huber W, Anders S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15: 550
59. Lozupone C, Knight R. (2005). UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235
60. Lozupone CA, Hamady M, Kelley ST, Knight R. (2007). Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73: 1576-1585
61. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Buchner A, et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371
62. Malmstrom RR, Coe A, Kettler GC, Martiny AC, Frias-Lopez J, Zinser ER, et al. (2010). Temporal dynamics of Prochlorococcus ecotypes in the Atlantic and Pacific oceans. ISME J 4: 1751-7362
63. Mary I, Cummings D, Biegala I. (2006). Seasonal dynamics of bacterioplankton community structure at a coastal station in the western English Channel. Aquat Microb Ecol 42: 119-126
64. McGillicuddy DJ, Anderson LA, Bates NR, Bibby T, Buesseler KO, Carlson CA, et al. (2007). Eddy/wind interactions stimulate extraordinary mid-ocean plankton blooms. Science 316: 1021-1026
65. Moore LR, Rocap G, Chisholm SW. (1998). Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393: 464-467
66. Moran MA, Miller WL. (2007). Resourceful heterotrophs make the most of light in the coastal ocean. Nat Rev Microbiol 5: 792-800
67. Morris RM, Vergin KL, Cho J-C, Rappé MS, Carlson CA, Giovannoni SJ. (2005). Temporal and spatial response of bacterioplankton lineages to annual convective overturn at the Bermuda Atlantic Time-series Study site. Limnol Oceanogr 50: 1687-1696
68. Murray AE, Preston CM, Massana R, Taylor LT, Blakis A, Wu K, et al. (1998). Seasonal and spatial variability of Bacterial and archaeal assemblages in the Coastal Waters near Anvers Island, Antarctica. Appl Environ Microbiol 64: 2585-2595
69. Noguchi H, Parker J, Takagi T. (2006). MetaGene: prokayrotic gene finding from environmental genome shotgun sequences. Nucleic Acids Res 34: 5623-5630
70. Ohman MD, Anderson GC, Ozturgut E. (1982). A multivariate analysis of planktonic interactions in the eastern tropical North Pacific. Deep Sea Res A 29: 1451-1469
71. Oksanen J, Kindt R, Pierre L, OHara B, Simpson GL, Solymos P, et al. (2013), vegan: Community Ecology Package, R package version 2.0. Available at: http://vegan.r-forge.r-project.org
72. Parsons RJ, Breitbart M, Lomas MW, Carlson CA. (2012). Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea. ISME J 6: 273-284
73. Price MN, Dehal PS, Arkin AP. (2009). FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26: 1641-1650
74. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, et al. (2007). SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196
75. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ. (2011). Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12: 38
76. Raes J, Letunic I, Yamada T, Jensen LJ, Bork P. (2011). Toward molecular trait-based ecology through integration of biogeochemical, geographical and metagenomic data. Mol Syst Biol 7: 473
77. Rich VI, Pham VD, Eppley J, Shi Y, DeLong EF. (2011). Time-series analyses of Monterey Bay coastal microbial picoplankton using a genome proxy microarray. Environ Microbiol 13: 116-134
78. Robidart JC, Church MJ, Ryan JP, Ascani F, Wilson ST, Bombar D. (2014). Ecogenomic sensor reveals controls on N2-fixing microorganisms in the North Pacific Ocean. ISME J 8: 1175-1185
79. Ruiz-González C, Simó R, Sommaruga R, Gasol JM. (2013). Away from darkness: a review on the effects of solar radiation on heterotrophic bacterioplankton activity. Front Microbiol 4: 131
80. Salazar G, Cornejo-Castillo FM, Benítez-Barrios V, Fraile-Nuez E, Álvarez-Salgado XA, Duarte CM, et al. (2016). Global diversity and biogeography of deep-sea pelagic prokaryotes. ISME J 10: 596-608
81. Schmidt T, DeLong E, Pace N. (1991). Analysis of a marine picoplankton community by 16S rRNA gene cloning and sequencing. J Bacteriol 173: 4371-4378
82. Sharma AK, Becker JW, Ottesen EA, Bryant JA, Duhamel S, Karl DM, et al. (2013). Distinct dissolved organic matter sources induce rapid transcriptional responses in coexisting populations of Prochlorococcus, Pelagibacter and the OM60 clade. Environ Microbiol 16: 2815-2830
83. Sharon I, Banfield JF. (2013). Genomes from metagenomics. Science 342: 1057-1058
84. Stewart FJ, Ottesen EA, DeLong EF. (2010). Development and quantitative analyses of a universal rRNAsubtraction protocol for microbial metatranscriptomics. ISME J 4: 896-907
85. Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G, et al. (2015). Structure and function of the global ocean microbiome. Science 348: 1261359
86. Swan BK, Martinez-Garcia M, Preston CM, Sczyrba A, Woyke T, Lamy D, et al. (2011). Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science 333: 1296-1300
87. Swan BK, Tupper B, Sczyrba A, Lauro FM, Martinez-Garcia M, González JM, et al. (2013). Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean. Proc Natl Acad Sci USA 110: 11463-11468
88. Treusch AH, Vergin KL, Finlay LA, Donatz MG, Burton RM, Carlson CA, et al. (2009). Seasonality and vertical structure of microbial communities in an ocean gyre. ISME J 3: 1148-1163
89. Tsai A-Y, Chiang P-P, Chang J, Gong GC. (2005). Seasonal diel variation of picoplankton and nanoplankton in a subtropical western Pacific coastal ecosystem. Limnol Oceanogr 50: 1221-1231
90. Tsai A-Y, Gong GC, Sanders RW, Chiang KP, Huang JK, Chan YF. (2012). Viral lysis and nanoflagellate grazing as factors controlling diel variations of Synechococcus spp. summer abundance in coastal waters of Taiwan. Aquat Microb Ecol 66: 159-167
91. Winn C, Chiswell S, Firing E, Karl DM, Lukas R (1992). Hawaii Ocean Time-series data report 2, 1990. University of Hawaii, HI, USA. SOEST Tech Rep 92-1
92. Winn CD, Campbell L, Christian JR, Letelier RM, Hebel D V, Dore JE, et al. (1995). Seasonal variability in the phytoplankton community of the North Pacific Subtropical Gyre. Global Biogeochem Cycles 9: 605-620
93. Wright T, Vergin K, Boyd P, Giovannoni S. (1997). A novel delta-subdivision proteobacterial lineage from the lower ocean surface layer. Appl Environ Microbiol 63: 1441-1448
94. Young RW, Carder KL, Betzer PR, Costello DK, Duce RA, DiTullio GR, et al. (1991). Atmospheric iron inputs and primary productivity: Phytoplankton responses in the North Pacific. Global Biogeochem Cycles 5: 119-134
95. Zhang B, Horvath S. (2005). A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol 4: Article 17
96. Zinser ER, Johnson ZI, Veneziano D, Chisholm SW. (2007). Influence of light and temperature on Prochlorococcus ecotype distributions in the Atlantic Ocean. Limnol Oceanogr 52: 2205-2220