Oceanographic structure drives the assembly processes of microbial eukaryotic communities

ISME Journal

Volumn 9, Issue , 2015, Pages 990-1002

  Monier, Adam ^a,b,d   Comte, Jérôme ^a,b,c   Babin, Marcel ^a,b   Forest, Alexandre ^a,b   Matsuoka, Atsushi ^a,b   Lovejoy, Connie ^a,b,c  

^a Université Laval   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c CENTRE D ÉTUDES NORDIQUES   (Canada)

^d UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL PRODUCTION; CHLOROPHYLL; EUKARYOTE; MARINE ECOSYSTEM; MICROBIAL COMMUNITY; RIVER DISCHARGE; SEA ICE;

ARCTIC OCEAN;

EUKARYOTA;

CHLOROPHYLL; SEA WATER;

ARCTIC; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; ENVIRONMENT; ENVIRONMENTAL ASPECTS AND RELATED PHENOMENA; EUKARYOTE; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYLOGENY; PHYLOGEOGRAPHY; PHYTOPLANKTON; RIVER; SALINITY; SEASON;

ARCTIC REGIONS; BIODIVERSITY; CHLOROPHYLL; ECOLOGICAL AND ENVIRONMENTAL PROCESSES; ENVIRONMENT; EUKARYOTA; PHYLOGENY; PHYLOGEOGRAPHY; PHYTOPLANKTON; RIVERS; SALINITY; SEASONS; SEAWATER;

EID: 84925066318     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2014.197     Document Type: Article

References (84)

1. Ardyna M, Gosselin M, Michel C, Poulin M, Tremblay J-E. (2011). Environmental forcing of phytoplankton community structure and function in the Canadian High Arctic: contrasting oligotrophic and eutrophic regions. Mar Ecol Prog Ser 442: 37-57.
2. Arrigo KR, Perovich DK, Pickart RS, Brown ZW, van Dijken GL, Lowry KE et al. (2012). Massive phytoplankton blooms under Arctic sea ice. Science 336: 1408-1408.
3. Balzano S, Gourvil P, Siano R, Chanoine M, Marie D, Lessard S et al. (2012a). Diversity of cultured photosynthetic flagellates in the northeast Pacific and Arctic Oceans in summer. Biogeosciences 11: 4553-4571.
4. Balzano S, Marie D, Gourvil P, Vaulot D. (2012b). Composition of the summer photosynthetic pico and nanoplankton communities in the Beaufort Sea assessed by T-RFLP and sequences of the 18S rRNA gene from flow cytometry sorted samples. ISME J 6: 1480-1498.
5. Berger SA, Stamatakis A. (2011). Aligning short reads to reference alignments and trees. Bioinformatics 27: 2068-2075.
6. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. (2010a). PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26: 266-267.
7. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al. (2010b). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
8. Carmack E, McLaughlin F. (2011). Towards recognition of physical and geochemical change in Subarctic and Arctic Seas. Prog Oceanogr 90: 90-104.
9. Carmack EC, Macdonald RW, Jasper S. (2004). Phytoplankton productivity on the Canadian Shelf of the Beaufort Sea. Mar Ecol Prog Ser 277: 37-50.
10. Carmack EC, Macdonald RW, Papadakis JE. (1989). Water mass structure and boundaries in the Mackenzie shelf estuary. J Geophys Res 94: 18043.
11. Cermeno P, Dutkiewicz S, Harris RP, Follows M, Schofield O, Falkowski PG. (2008). The role of nutricline depth in regulating the ocean carbon cycle. Proc Natl Acad Sci USA 105: 20344-20349.
12. Chappell PD, Whitney LP, Haddock TL, Menden-Deuer S, Roy EG, Wells ML et al. (2013). Thalassiosira spp. Community composition shifts in response to chemical and physical forcing in the northeast Pacific Ocean. Front Microbiol 4: 273.
13. Chase JM. (2003). Community assembly: when should history matter? Oecologia 136: 489-498.
14. Chase JM, Leibold MA. (2002). Spatial scale dictates the productivity-biodiversity relationship. Nature 416: 427-430.
15. Chase JM, Myers JA. (2011). Disentangling the importance of ecological niches from stochastic processes across scales. Philos Trans R Soc Ser B 366: 2351-2363.
16. Chen J, Bittinger K, Charlson ES, Hoffmann C, Lewis J, Wu GD et al. (2012). Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics 28: 2106-2113.
17. Clarke KR, Ainsworth M. (1993). A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 92: 205-205.
18. Comeau AM, Li WKW, Tremblay J-E, Carmack EC, Lovejoy C. (2011). Arctic Ocean microbial community structure before and after the 2007 record sea ice minimum. PLoS One 6: e27492.
19. Cuvelier ML, Ortiz A, Kim E, Moehlig H, Richardson DE, Heidelberg JF et al. (2008). Widespread distribution of a unique marine protistan lineage. Environ Microbiol 10: 1621-1634.
20. Ding Y, Zang R, Letcher SG, Liu S, He F. (2011). Disturbance regime changes the trait distribution, phylogenetic structure and community assembly of tropical rain forests. Oikos 121: 1263-1270.
21. Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH. (2009). Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4: 337-345.
22. Edgar RC. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
23. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
24. Eisenhauer N, Scheu S, Jousset A. (2012). Bacterial diversity stabilizes community productivity. PLoS One 7: e34517.
25. Forest A, Babin M, Stemmann L, Picheral M, Sampei M, Fortier L et al. (2013). Ecosystem function and particle flux dynamics across the Mackenzie Shelf (Beaufort Sea, Arctic Ocean): an integrative analysis of spatial variability and biophysical forcings. Biogeosciences 10: 2833-2866.
26. Fu L, Niu B, Zhu Z, Wu S, Li W. (2012). CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28: 3150-3152.
27. Goslee SC, Urban DL. (2007). The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22: 1-19.
28. Gotelli NJ, Entsminger GL. (2003). Swap algorithms in null model analysis. Ecology 84: 532-535.
29. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH. (2012). Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10: 497-506.
30. Harding T, Jungblut AD, Lovejoy C, Vincent WF. (2011). Microbes in high Arctic snow and implications for the cold biosphere. Appl Environ Microb 77: 3234-3243.
31. Harrell FE Jr. (2008). Hmisc: Harrell Miscellaneous. R package version 3.12-2. Availabe at:http://cran. r-project.org/package=Hmisc (accessed 2 October 2014).
32. Helmus MR, Keller WB, Paterson MJ, Yan ND, Cannon CH, Rusak JA. (2010). Communities contain closely related species during ecosystem disturbance. Ecol Lett 13: 162-174.
33. Hill VJ, Matrai PA, Olson E, Suttles S, Steele M, Codispoti LA et al. (2013). Synthesis of integrated primary production in the Arctic Ocean: II. In situ and remotely sensed estimates. Prog Oceanogr 110: 107-125.
34. Horner-Devine MC, Leibold MA, Smith VH, Bohannan BJM. (2003). Bacterial diversity patterns along a gradient of primary productivity. Ecol Lett 6: 613-622.
35. Horner-Devine MC, Bohannan BJM. (2006). Phylogenetic clustering and overdispersion in bacterial communities. Ecology 87: 100-108.
36. Jakobsson M, Mayer L, Coakley B, Dowdeswell JA, Forbes S, Fridman B et al. (2012). The international bathymetric chart of the Arctic Ocean (IBCAO) version 3.0. Geophys Res Lett 39: L12609.
37. Katoh K, Frith MC. (2012). Adding unaligned sequences into an existing alignment using MAFFT and LAST. Bioinformatics 28: 3144-3146.
38. Katoh K, Standley DM. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772-780.
39. Keane TM, Creevey CJ, Pentony MM, Naughton TJ, Mclnerney JO. (2006). Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol. 6: 29.
40. Kembel SW. (2009). Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests. Ecol Lett 12: 949-960.
41. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD et al. (2010). Picante: R tools for integrating phylogenies and ecology. Bioinfor-matics 26: 1463-1464.
42. Klausmeier CA, Litchman E. (2001). Algal games: the vertical distribution of phytoplankton in poorly mixed water columns. Limnol Oceanogr 46: 1998-2007.
43. Leibold MA, Economo EP, Peres-Neto P. (2010). Metacommunity phylogenetics: separating the roles of environmental filters and historical biogeography. Ecol Lett 13: 1290-1299.
44. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF et al. (2004). The meta-community concept: a framework for multi-scale community ecology. Ecol Lett 7: 601-613.
45. Li WKW, McLaughlin FA, Lovejoy C, Carmack EC. (2009). Smallest algae thrive as the Arctic Ocean freshens. Science 326: 539.
46. Lovejoy C. (2012). Polar marine microbiology. In: Miller RV, Whyte LG (eds) Polar Microbiology: Life in a Deep Freeze. ASM Press: Washington, DC, pp 1-17.
47. Lovejoy C, Potvin M. (2011). Microbial eukaryotic distribution in a dynamic Beaufort Sea and the Arctic Ocean. J Plankton Res 33: 431-444.
48. Lovejoy C, Vincent WF, Bonilla S, Roy S, Martineau M-J, Terrado R et al. (2007). Distribution, phylogeny, and growth of cold-Adapted picoprasinophytes in Arctic Seas. J Phycol 43: 78-89.
49. Lozupone C, Knight R. (2005). UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microb 71: 8228-8235.
50. Macdonald RW, Carmack EC, McLaughlin FA, Iseki K, Macdonald DM, O'Brien MC. (1989). Composition and modification of water masses in the Mackenzie shelf estuary. J Geophys Res 94: 18057.
51. Martin J, Tremblay JE, Gagnon J, Tremblay G, Lapoussière A, Jose C et al. (2010). Prevalence, structure and properties of subsurface chlorophyll maxima in Canadian Arctic waters. Mar Ecol Prog Ser 412: 69-84.
52. Martin J, Tremblay JE, Price NM. (2012). Nutritive and photosynthetic ecology of subsurface chlorophyll maxima in Canadian Arctic waters. Biogeosciences 9: 5353-5371.
53. Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL et al. (2006). Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4: 102-112.
54. Martiny JBH, Eisen JA, Penn K, Allison SD, Horner-Devine MC. (2011). Drivers of bacterial beta-diversity depend on spatial scale. Proc Natl Acad Sci USA 108: 7850-7854.
55. Matsuoka A, Bricaud A, Benner R, Para J, Sempéré R, Prieur L et al. (2012). Tracing the transport of colored dissolved organic matter in water masses of the Southern Beaufort Sea: relationship with hydrographic characteristics. Biogeosciences 9: 925-940.
56. Mayfield MM, Levine JM. (2010). Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol Lett 13: 1085-1093.
57. McKie-Krisberg ZM, Sanders RW. (2014). Phagotrophy by the picoeukaryotic green alga Micromonas: implications for Arctic Oceans. ISME J 8: 1953-1961.
58. McLaughlin FA, Carmack EC. (2010). Deepening of the nutricline and chlorophyll maximum in the Canada Basin interior, 2003-2009. Geophys Res Lett 37: article L24602.
59. Monier A, Terrado R, Thaler M, Comeau AM, Medrinal E, Lovejoy C. (2013). Upper Arctic Ocean water masses harbor distinct communities of heterotrophic flagellates. Biogeosciences 10: 4273-4286.
60. Nelson CE, Carlson CA, Ewart CS, Halewood ER. (2013). Community differentiation and population enrichment of Sargasso Sea bacterioplankton in the euphotic zone of a mesoscale mode-water eddy. Environ Microbiol 16: 871-887.
61. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB et al. (2007). Vegan: Community Ecology Package. R package version 2.0-8. Available at: http://cran.r-project.org/package=vegan (accessed 2 October 2014).
62. Peres-Neto PR, Legendre P. (2010). Estimating and controlling for spatial structure in the study of ecological communities. Global Ecol Biogeog 19: 174-184.
63. Peterson BJ, Holmes RM, McClelland JW, Vörösmarty CJ, Lammers RB, Shiklomanov AI et al. (2002). Increasing river discharge to the Arctic Ocean. Science 298: 2171-2173.
64. Pontarp M, Sjöstedt J, Lundberg P. (2013). Experimentally, induced habitat filtering in marine bacterial communities. Mar Ecol Prog Ser 477: 77-86.
65. Post E, Bhatt US, Bitz CM, Brodie JF, Fulton TL, Hebblewhite M et al. (2013). Ecological consequences of sea-ice decline. Science 341: 519-524.
66. Price MN, Dehal PS, Arkin AP. (2010). FastTree 2-Approximately maximum-likelihood trees for large alignments. PLoS One 5: e9490.
67. 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.
68. Rainville L, Lee CM, Woodgate RA. (2011). Impact of wind-driven mixing in the Arctic Ocean. Oceanography 24: 136-145.
69. Ricklefs RE. (2007). History and diversity: explorations at the intersection of ecology and evolution. Am Nat 170: S56-S70.
70. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75: 7537-7541.
71. Screen JA, Simmonds I. (2010). The central role of diminishing sea ice in recent Arctic temperature amplification. Nature 464: 1334-1337.
72. Seenivasan R, Sausen N, Medlin LK, Melkonian M. (2013). Picomonas judraskeda gen. et sp. Nov.: the first identified member of the Picozoa phylum nov., a widespread group of picoeukaryotes, formerly known as 'Picobiliphytes'. PLoS One 8: e59565.
73. Sherr EB, Sherr BF, Wheeler PA, Thompson K. (2003). Temporal and spatial variation in stocks of autotrophic and heterotrophic microbes in the upper water column of the central Arctic Ocean. Deep-Sea Res Part I 50: 557-571.
74. Smith VH. (2007). Microbial diversity-productivity relationships in aquatic ecosystems. FEMS Microbiol Ecol 62: 181-186.
75. Soininen J, Korhonen JJ, Karhu J, Vetterli A. (2011). Disentangling the spatial patterns in community composition of prokaryotic and eukaryotic lake plankton. Limnol Oceanogr 56: 508-520.
76. Stamatakis A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
77. Stegen JC, Lin X, Konopka AE, Fredrickson JK. (2012). Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J 6: 1653-1664.
78. Tremblay J-E, Gagnon J. (2009). The effects of irradiance and nutrient supply on the productivity of Arctic waters: a perspective on climate change. In: Nihoul JCJ, Kostianoy AG (eds) NATO Science for Peace and Security Series C: Environmental Security. Springer: Dordrecht, Netherlands, pp 73-93.
79. Waide RB, Willig MR, Steiner CF, Mittelbach G, Gough L, Dodson SI et al. (1999). The relationship between productivity and species richness. Annu Rev Ecol Syst 30: 257-300.
80. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ. (2002). Phylogenies and community ecology. Annu Rev Ecol Syst 33: 475-505.
81. Wheeler PA, Gosselin M, Sherr E, Thibaultc D, Kirchman DL, Benner R et al. (1996). Active cycling of organic carbon in the central Arctic Ocean. Nature 380: 697-699.
82. White JR, Nagarajan N, Pop M. (2009). Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5: e1000352.
83. Williams WJ, Carmack EC, Shimada K, Melling H, Aagaard K, Macdonald RW et al. (2006). Joint effects of wind and ice motion in forcing upwelling in Mackenzie Trough, Beaufort Sea. Cont Shelf Res 26: 2352-2366.
84. Yoon HS, Price DC, Stepanauskas R, Rajah VD, Sieracki ME, Wilson WH et al. (2011). Single-cell genomics reveals organismal interactions in uncultivated marine protists. Science 332: 714-717.