Plankton networks driving carbon export in the oligotrophic ocean

Nature

Volumn 532, Issue 7600, 2016, Pages 465-470

  Guidi, Lionel ^a,b   Chaffron, Samuel ^c,d,e   Bittner, Lucie ^a,f,v   Eveillard, Damien ^g   Larhlimi, Abdelhalim ^g   Roux, Simon ^h,u   Darzi, Youssef ^c,d   Audic, Stephane ^a   Berline, Léo ^a   Brum, Jennifer R ^h,u   Coelho, Luis Pedro ⁱ   Espinoza, Julio Cesar Ignacio ^h   Malviya, Shruti ^f,w   Sunagawa, Shinichi ⁱ   Dimier, Céline ^a   Kandels Lewis, Stefanie ⁱ   Picheral, Marc ^a   Poulain, Julie ^j   Searson, Sarah ^a,b   Stemmann, Lars ^a   Not, Fabrice ^a   Hingamp, Pascal ^k   Speich, Sabrina ^f   Follows, Mick ^l   Karp Boss, Lee ^m   Boss, Emmanuel ^m   Ogata, Hiroyuki ⁿ   Pesant, Stephane ^o   Weissenbach, Jean ^j,p,q   Wincker, Patrick ^j,p,q   Acinas, Silvia G ^r   Bork, Peer ^i,s   De Vargas, Colomban ^a   Iudicone, Daniele ^t   Sullivan, Matthew B ^h,u   Raes, Jeroen ^c,d,e   Karsenti, Eric ^f,i   Bowler, Chris ^f   Gorsky, Gabriel ^a   more..

^a SORBONNE UNIVERSITÉ   (France)

^b UNIVERSITY OF HAWAII   (United States)

^c REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^e VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^f ECOLE NORMALE SUPÉRIEURE   (France)

^g UNIVERSITÉ DE NANTES   (France)

^h The University of Arizona   (United States)

ⁱ EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^j CEA Fontenay aux Roses Bâtiment 61   (France)

^k CNRS Aix Marseille University   (France)

^l MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^m UNIVERSITY OF MAINE   (United States)

ⁿ KYOTO UNIVERSITY   (Japan)

^o UNIVERSITY OF BREMEN   (Germany)

^p CNRS   (France)

^q UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^r INSTITUT DE CIÈNCIES DEL MAR   (Spain)

^s MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^t STAZIONE ZOOLOGICA ANTON DOHRN   (Italy)

^u OHIO STATE UNIVERSITY   (United States)

^v AIX MARSEILLE UNIVERSITY   (France)

^w NATIONAL INSTITUTE OF OCEANOGRAPHY   (India)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CHLOROPHYLL; SEA WATER;

BIOLOGICAL UPTAKE; CARBON DIOXIDE; CARBON SEQUESTRATION; CHLOROPHYLL; DEEP SEA; ECOSYSTEM STRUCTURE; OLIGOTROPHIC ENVIRONMENT; ORGANIC CARBON; PARASITE; PHOTOSYNTHESIS; PLANKTON; RADIOLARIA; RELATIVE ABUNDANCE;

ALVEOLATA; ARTICLE; BACTERIAL GENE; ENVIRONMENTAL PARAMETERS; GENE FUNCTION; METAGENOMICS; MICROBIAL COMMUNITY; NONHUMAN; NUTRIENT; PLANKTON; PRIORITY JOURNAL; SEA; SYNECHOCOCCUS; VIRUS GENE; AQUATIC SPECIES; CHEMISTRY; DINOFLAGELLATE; ECOSYSTEM; GENETICS; GEOGRAPHY; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PARASITOLOGY; PHOTOSYNTHESIS; TRAVEL; VIROLOGY;

BACTERIA (MICROORGANISMS); SYNECHOCOCCUS;

AQUATIC ORGANISMS; CARBON; CHLOROPHYLL; DINOFLAGELLIDA; ECOSYSTEM; EXPEDITIONS; GENES, BACTERIAL; GENES, VIRAL; GEOGRAPHY; OCEANS AND SEAS; PHOTOSYNTHESIS; PLANKTON; SEAWATER; SYNECHOCOCCUS;

EID: 84961057176     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16942     Document Type: Article

References (68)

1. Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237-240 (1998).
2. Boyd, P. W. & Newton, P. Evidence of the potential influence of planktonic community structure on the interannual variability of particulate organiccarbon flux. Deep Sea Res. Part I Oceanogr. Res. Pap. 42, 619-639 (1995).
3. Guidi, L. et al. Effects of phytoplankton community on production, size, and export of large aggregates: a world-ocean analysis. Limnol. Oceanogr. 54, 1951-1963 (2009).
4. Kwon, E. Y., Primeau, F. & Sarmiento, J. L. The impact of remineralization depth on the air-sea carbon balance. Nature Geosci. 2, 630-635 (2009).
5. IPCC. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. (Cambridge University Press, 2013).
6. Kitano, H. Biological robustness. Nature Rev. Genet. 5, 826-837 (2004).
7. Suweis, S., Simini, F., Banavar, J. R. & Maritan, A. Emergence of structural and dynamical properties of ecological mutualistic networks. Nature 500, 449-452 (2013).
8. Chow, C. E. T., Kim, D. Y., Sachdeva, R., Caron, D. A. & Fuhrman, J. A. Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists. ISME J. 8, 816-829 (2014).
9. Fuhrman, J. A. Microbial community structure and its functional implications. Nature 459, 193-199 (2009).
10. Lima-Mendez, G. et al. Determinants of community structure in the global plankton interactome. Science 348, (2015).
11. Giering, S. L. C. et al. Reconciliation of the carbon budget in the ocean's twilight zone. Nature 507, 480-483 (2014).
12. Azam, F. Microbial control of oceanic carbon flux: the plot thickens. Science 280, 694-696 (1998).
13. Agusti, S. et al. Ubiquitous healthy diatoms in the deep sea confirm deep carbon injection by the biological pump. Nature Commun. 6, 7608 (2015).
14. Sancetta, C., Villareal, T. & Falkowski, P. Massive fluxes of rhizosolenid diatoms-A common occurrence. Limnol. Oceanogr. 36, 1452-1457 (1991).
15. Scharek, R., Tupas, L. M. & Karl, D. M. Diatom fluxes to the deep sea in the oligotrophic north Pacific gyre at station ALOHA. Mar. Ecol. Prog. Ser. 182, 55-67 (1999).
16. Omand, M. M. et al. Eddy-driven subduction exports particulate organic carbon from the spring bloom. Science 348, 222-225 (2015).
17. Richardson, T. L. & Jackson, G. A. Small phytoplankton and carbon export from the surface ocean. Science 315, 838-840 (2007).
18. Steinberg, D. K. et al. Bacterial vs. zooplankton control of sinking particle flux in the ocean's twilight zone. Limnol. Oceanogr. 53, 1327-1338 (2008).
19. Turner, J. T. Zooplankton fecal pellets, marine snow, phytodetritus and the ocean's biological pump. Prog. Oceanogr. 130, 205-248 (2015).
20. Karsenti, E. et al. A holistic approach to marine eco-systems biology. PLoS Biol. 9, (2011).
21. Strom, S. L. Microbial ecology of ocean biogeochemistry: a community perspective. Science 320, 1043-1045 (2008).
22. Worden, A. Z. et al. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science 347, 1257594 (2015).
23. Sunagawa, S. et al. Structure and function of the global ocean microbiome. Science 348, 1261359 (2015).
24. de Vargas, C. et al. Eukaryotic plankton diversity in the sunlit ocean. Science 348, 1261605 (2015).
25. Brum, J. R. et al. Patterns and ecological drivers of ocean viral communities. Science 348, 1261498 (2015).
26. Bork, P. et al. Tara Oceans studies plankton at planetary scale. Science 348, 873 (2015).
27. Honjo, S., Manganini, S. J., Krishfield, R. A. & Francois, R. Particulate organic carbon fluxes to the ocean interior and factors controlling the biological pump: A synthesis of global sediment trap programs since 1983. Prog. Oceanogr. 76, 217-285 (2008).
28. Henson, S. A., Sanders, R. & Madsen, E. Global patterns in efficiency of particulate organic carbon export and transfer to the deep ocean. Glob. Biogeochem. Cycles 26, (2012).
29. Lě Cao, K. A., Rossouw, D., Robert-Granié, C. & Besse, P. A sparse PLS for variable selection when integrating omics data. Stat. Appl. Genet. Mol. Biol. 7, 35 (2008).
30. Chaffron, S., Rehrauer, H., Pernthaler, J. & von Mering, C. A global network of coexisting microbes from environmental and whole-genome sequence data. Genome Res. 20, 947-959 (2010).
31. Faust, K. & Raes, J. Microbial interactions: from networks to models. Nature Rev. Microbiol. 10, 538-550 (2012).
32. Aylward, F. O. et al. Microbial community transcriptional networks are conserved in three domains at ocean basin scales. Proc. Natl Acad. Sci. 112, 5443-5448 (2015).
33. Langfelder, P. & Horvath, S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9 (2008).
34. Fontanez, K. M., Eppley, J. M., Samo, T. J., Karl, D. M. & DeLong, E. F. Microbial community structure and function on sinking particles in the North Pacific Subtropical Gyre. Front. Microbiol. 6, (2015).
35. Thomas, T. et al. Analysis of the Pseudoalteromonas tunicata genome reveals properties of a surface-Associated life style in the marine environment. PLoS ONE 3, (2008).
36. Azam, F. & Malfatti, F. Microbial structuring of marine ecosystems. Nature Rev. Microbiol. 5, 782-791 (2007).
37. Shi, Y., Tyson, G. W. & DeLong, E. F. Metatranscriptomics reveals unique microbial small RNAs in the ocean's water column. Nature 459, 266-269 (2009).
38. Yooseph, S. et al. The Sorcerer II Global Ocean Sampling expedition: expanding the universe of protein families. PLoS Biol. 5, e16 (2007).
39. Suttle, C. A. Marine viruses-major players in the global ecosystem. Nature Rev. Microbiol. 5, 801-812 (2007).
40. Weinbauer, M. G. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28, 127-181 (2004).
41. Finkel, Z. V. et al. Phytoplankton in a changing world: cell size and elemental stoichiometry. J. Plankton Res. 32, 119-137 (2010).
42. Sommer, U. & Lewandowska, A. Climate change and the phytoplankton spring bloom: warming and overwintering zooplankton have similar effects on phytoplankton. Glob. Change Biol. 17, 154-162 (2011).
43. Behrenfeld, M. J. et al. Climate-driven trends in contemporary ocean productivity. Nature 444, 752-755 (2006).
44. DeLong, E. F. et al. Community genomics among stratified microbial assemblages in the ocean's interior. Science 311, 496-503 (2006).
45. Gianoulis, T. A. et al. Quantifying environmental adaptation of metabolic pathways in metagenomics. Proc. Natl Acad. Sci. USA 106, 1374-1379 (2009).
46. Tilman, D. et al. The influence of functional diversity and composition on ecosystem processes. Science 277, 1300-1302 (1997).
47. Wymore, A. S. et al. Genes to ecosystems: exploring the frontiers of ecology with one of the smallest biological units. New Phytol. 191, 19-36 (2011).
48. Picheral, M. et al. Vertical profiles of environmental parameters measured on discrete water samples collected with Niskin bottles during the Tara Oceans expedition 2009-2013. PANGAEA http://dx.doi.org/10.1594/PANGAEA.836319 (2014).
49. Picheral, M. et al. Vertical profiles of environmental parameters measured from physical, optical and imaging sensors during Tara Oceans expedition 2009-2013. PANGAEA http://dx.doi.org/10.1594/PANGAEA.836321 (2014).
50. Chaffron, S. et al. Contextual environmental data of selected samples from the Tara Oceans Expedition (2009-2013). PANGAEA http://dx.doi.org/10.1594/PANGAEA.840718 (2014).
51. Pesant, S. et al. Open science resources for the discovery and analysis of Tara Oceans data. Sci. Data 2, 150023 (2015).
52. Picheral, M. et al. The Underwater Vision Profiler 5: An advanced instrument for high spatial resolution studies of particle size spectra and zooplankton. Limnol. Oceanogr. Methods 8, 462-473 (2010).
53. Behrenfeld, M. J. & Falkowski, P. G. Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol. Oceanogr. 42, 1-20 (1997).
54. McCave, I. N. Size spectra and aggregation of suspended particles in the deep ocean. Deep Sea Res. Part I Oceanogr. Res. Pap. 31, 329-352 (1984).
55. Sheldon, R. W., Prakash, A. & Sutcliff, W. H. Size distribution of particles in ocean. Limnol. Oceanogr. 17, 327-340 (1972).
56. Guidi, L. et al. Relationship between particle size distribution and flux in the mesopelagic zone. Deep Sea Res. Part I Oceanogr. Res. Pap. 55, 1364-1374 (2008).
57. Logares, R. et al. 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 (2014).
58. Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590-D596 (2013).
59. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).
60. Kultima, J. R. et al. MOCAT: a metagenomics assembly and gene prediction toolkit. PLoS ONE 7, e47656 (2012).
61. Hingamp, P. et al. Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes. ISME J. 7, 1678-1695 (2013).
62. Zhao, Y., Tang, H. & Ye, Y. RAPSearch2: a fast and memory-efficient protein similarity search tool for next-generation sequencing data. Bioinformatics 28, 125-126 (2012).
63. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nature Methods 9, 357-359 (2012).
64. Shen, H. P. & Huang, J. H. Z. Sparse principal component analysis via regularized low rank matrix approximation. J. Multivar. Anal. 99, 1015-1034 (2008).
65. Langfelder, P. & Horvath, S. Eigengene networks for studying the relationships between co-expression modules. BMC Syst. Biol. 1, 54 (2007).
66. Li, A. & Horvath, S. Network neighborhood analysis with the multi-node topological overlap measure. Bioinformatics 23, 222-231 (2007).
67. Chong, I. G. & Jun, C. H. Performance of some variable selection methods when multicollinearity is present. Chemometr. Intell. Lab. 78, 103-112 (2005).
68. Mevik, B. H. & Wehrens, R. The pls package: Principal component and partial least squares regression in R. J. Stat. Softw. 18, 1-23 (2007).