Abstract
Metagenomic approaches have revealed unprecedented genetic diversity within microbial communities across vast expanses of the world’s oceans. Linking this genetic diversity with key metabolic and cellular activities of microbial assemblages is a fundamental challenge. Here we report on a collaborative effort to design MicroTOOLs (Microbiological Targets for Ocean Observing Laboratories), a high-density oligonucleotide microarray that targets functional genes of diverse taxa in pelagic and coastal marine microbial communities. MicroTOOLs integrates nucleotide sequence information from disparate data types: genomes, PCR-amplicons, metagenomes, and metatranscriptomes. It targets 19 400 unique sequences over 145 different genes that are relevant to stress responses and microbial metabolism across the three domains of life and viruses. MicroTOOLs was used in a proof-of-concept experiment that compared the functional responses of microbial communities following Fe and P enrichments of surface water samples from the North Pacific Subtropical Gyre. We detected transcription of 68% of the gene targets across major taxonomic groups, and the pattern of transcription indicated relief from Fe limitation and transition to N limitation in some taxa. Prochlorococcus (eHLI), Synechococcus (sub-cluster 5.3) and Alphaproteobacteria SAR11 clade (HIMB59) showed the strongest responses to the Fe enrichment. In addition, members of uncharacterized lineages also responded. The MicroTOOLs microarray provides a robust tool for comprehensive characterization of major functional groups of microbes in the open ocean, and the design can be easily amended for specific environments and research questions.
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References
Abell GCJ, Robert SS, Frampton DMF, Volkman JK, Rizwi F et al (2012). High-throughput analysis of ammonia oxidiser community composition via a novel, amoA-based functional gene array. PLoS One 7: e51542.
Ahlgren NA, Rocap G . (2012). Diversity and distribution of marine Synechococcus: multiple gene phylogenies for consensus classification and development of qPCR assays for sensitive measurement of clades in the ocean. Front Microbio 3: 213.
Allen LZ, Allen EE, Badger JH, McCrow JP, Paulsen IT, Elbourne LDH et al (2012). Influence of nutrients and currents on the genomic composition of microbes across an upwelling mosaic. ISME J 6: 1403–1414.
Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH et al (2004). The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306: 79–86.
Azam F, Malfatti F . (2007). Microbial structuring of marine ecosystems. Nat Rev Microbiol 5: 782–791.
Bagg A, Neilands JB . (1987). Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli. Biochemistry 26: 5471–5477.
Bai S, Li J, He Z, Van Nostrand JD, Tian Y, Lin G et al (2013). GeoChip-based analysis of the functional gene diversity and metabolic potential of soil microbial communities of mangroves. Appl Microbiol Biotechnol 97: 7035–7048.
Bauer DF . (1972). Constructing confidence sets using rank statistics. J Am Stat Assoc 67: 687–690.
Benjamini Y, Hochberg Y . (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodological) 57: 289–300.
Björkman K, Duhamel S, Karl DM . (2012). Microbial group specific uptake kinetics of inorganic phosphate and adenosine-5’-triphosphate (ATP) in the North Pacific Subtropical Gyre. Front Microbiol 3: 189 doi:10.3389/fmicb.2012.00189.
Bouskill NJ, Eveillard D, O'Mullan G, Jackson GA, Ward BB . (2011). Seasonal and annual reoccurrence in betaproteobacterial ammonia-oxidizing bacterial population structure. Environ Microbiol 13: 872–886.
Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A et al (2008). The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456: 239–244.
Boyle EA, Bergquist BA, Kayser RA, Mahowald N . (2005). Iron, manganese, and lead at Hawaii Ocean Time-series station ALOHA: temporal variability and an intermediate water hydrothermal plume. Geochim Cosmochim Acta 69: 933–952.
Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C et al (2001). Minimum information about a microarray experiment (MIAME)—toward standards for microarray data. Nat Genet 29: 365–371.
Brodie EL, DeSantis TZ, Joyner DC, Baek SM, Larsen JT, Andersen GL et al (2006). Application of a high-density oligonucleotide microarray approach to study bacterial population dynamics during uranium reduction and reoxidation. Appl Environ Microbiol 72: 6288–6298.
Brown MV, Lauro FM, DeMaere MZ, Muir L, Wilkins D, Thomas T et al (2012). Global biogeography of SAR11 marine bacteria. Mol Syst Biol 8: 595.
Bulow SE, Francis CA, Jackson GA, Ward BB . (2008). Sediment denitrifier community composition and nirS gene expression investigated with functional gene microarrays. Environ Microbiol 10: 3057–3069.
Cembella AD, Antia NJ, Harrison PJ . (1982). The utilization of inorganic and organic phosphorous compounds as nutrients by eukaryotic microalgae: a multidisciplinary perspective: Part I. Crit Rev Microbiol 10: 317–391.
Chen F, Wang K, Kan JJ, Bachoon DS, Lu JR, Lau S et al (2004). Phylogenetic diversity of Synechococcus in the Chesapeake Bay revealed by ribulose-1,5-bisphosphate carboxylase-oxygenase (RuBisCO) large subunit gene (rbcL) sequences. Aquat Microb Ecol 36: 153–164.
Chung WH, Rhee SK, Wan XF, Bae JW, Quan ZX, Park YH . (2005). Design of long oligonucleotide probes for functional gene detection in a microbial community. Bioinformatics 21: 4092–4100.
Church MJ, Mahaffey C, Letelier RM, Lukas R, Zehr JP, Karl DM . (2009). Physical forcing of nitrogen fixation and diazotroph community structure in the North Pacific Subtropical Gyre. Glob Biogeochem Cycles 23: GB2020.
Church MJ, Short CM, Jenkins BD, Karl DM, Zehr JP . (2005). Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean. Appl Environ Microbiol 71: 5362–5370.
Coleman ML, Chisholm SW . (2010). Ecosystem-specific selection pressures revealed through comparative population genomics. Proc Natl Acad Sci USA 107: 18634–18639.
DeLong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard NU et al (2006). Community genomics among stratified microbial assemblages in the ocean's interior. Science 311: 496–503.
Dugat-Bony E, Peyretaillade E, Parisot N, Biderre-Petit C, Jaziri F, Hill D et al (2011). Detecting unknown sequences with DNA microarrays: explorative probe design strategies. Environ Microbiol 14: 356–371.
Dupont CL, Barbeau K, Palenik B . (2008). Ni uptake and limitation in marine Synechococcus strains. Appl Environ Micro 74: 23–31.
Dyhrman ST, Haley ST . (2006). Phosphorus scavenging in the unicellular marine diazotroph Crocosphaera watsonii. Appl Environ Microbiol 72: 1452–1458.
Frias-Lopez J, Shi Y, Tyson GW, Coleman ML, Schuster SC, Chisholm SW et al (2008). Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci USA 105: 3805–3810.
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.
Fuller NJ, West NJ, Marie D, Yallop M, Rivlin T, Post AF et al (2005). Dynamics of community structure and phosphate status of picocyanobacterial populations in the Gulf of Aqaba, Red Sea. Limnol Oceanogr 50: 363–375.
Gautier L, Cope L, Bolstad BM, Irizarry RA . (2004). affy analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307–315.
Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S et al (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
Giovannoni SJ, Vergin KL . (2012). Seasonality in ocean microbial communities. Science 335: 671–676.
Grabowski M, Church M, Karl D . (2008). Nitrogen fixation rates and controls at Stn. ALOHA. Aquat Microb Ecol 52: 175–183.
He Z, Deng Y, Van Nostrand JD, Tu Q, Xu M, Hemme CL et al (2010). GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity. ISME J 4: 1167–1179.
He Z, Gentry TJ, Schadt CW, Wu L, Liebich J, Chong SC et al (2007). GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME J 1: 67–77.
Hernández JA, Muro-Pastor AM, Flores E, Bes MT, Peleato ML, Fillat MF . (2006). Identification of a furA cis antisense RNA in the cyanobacterium Anabaena sp. PCC 7120. J Mol Biol 355: 325–334.
Hewson I, Poretsky RS, Tripp HJ, Montoya JP, Zehr JP . (2010). Spatial patterns and light-driven variation of microbial population gene expression in surface waters of the oligotrophic open ocean. Environ Microbiol 12: 1940–1956.
Holtzendorff J, Marie D, Post AF, Partensky F, Rivlin A, Hess WR . (2002). Synchronized expression of ftsZ in natural Prochlorococcus populations of the Red Sea. Environ. Microbiol 4: 644–653.
Huang S, Wilhelm SW, Harvey HR, Taylor K, Jiao N, Chen F . (2012). Novel lineages of Prochlorococcus and Synechococcus in the global oceans. ISME J 6: 285–297.
Huang Y, Niu B, Gao Y, Fu L, Li W . (2010). CD-HIT suite: a web server for clustering and comparing biological sequences. Bioinformatics 26: 680–682.
Hutchins DA, Witter AE, Butler A, Luther GW . (1999). Competition among marine phytoplankton for different chelated iron species. Nature 400: 858–861.
Ilikchyan IN, McKay RM, Zehr JP, Dyhrman ST, Bullerjahn GS . (2009). Detection and expression of the phosphonate transporter gene phnD in marine and freshwater picocyanobacteria. Environ Microbiol 11: 1314–1324.
Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U et al (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249–264.
Jansson M . (1988). Phosphate uptake and utilization by bacteria and algae. Hydrobiologia 170: 177–189.
Kamennaya NA, Post AF . (2011). Characterization of cyanate metabolism in marine Synechococcus and Prochlorococcus spp. Appl Environ Microbiol 77: 291–301.
Karl DM, Björkman KM, Dore JE, Fujieki L, Hebel DV, Houlihan T et al (2001). Ecological nitrogen-to-phosphorus stoichiometry at Station ALOHA. Deep-Sea Res II 48: 1529–1566.
Karl DM, Letelier R . (2008). Nitrogen fixation-enhanced carbon sequestration in low nitrate, low chlorophyll seascapes. Mar Ecol Prog Ser 364: 257–268.
Karl DM, Letelier R, Tupas L, Dore J, Christian J, Hebel D . (1997). The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388: 533–538.
Karl DM, Lukas R . (1996). The Hawaii ocean time-series (HOT) program: background, rationale, and field implementation. Deep-Sea Res II 43: 129–156.
Kolber ZS, Prasil O, Falkowski PG . (1998). Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta Bioenerg 1367: 88–106.
Laws EA . (1991). Photosynthetic quotients, new production and net community production in the open ocean. Deep-Sea Res Oceanogr A 38: 143–167.
Lemire A, Lea K, Batten D, Gu J, Whitley P, Bramlett K . (2011). Development of ERCC RNA spike-in control mixes. J Biomol Tech 22: S46.
Li C, Wong WH . (2001). Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA 98: 31–36.
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.
Lindell D, Post AF . (2001). Ecological aspects of ntcA gene expression and its use as an indicator of the nitrogen status of marine Synechococcus spp. Appl Environ Microbiol 67: 3340–3349.
Lu Z, Deng Y, Van Nostrand JD, He Z, Voordeckers J, Zhou A et al (2012). Microbial gene functions enriched in the Deepwater Horizon deep-sea oil plume. ISME J 6: 451–460.
Mann EL, Chisholm SW . (2000). Iron limits the cell division rate of Prochlorococcus in the eastern equatorial Pacific. Limnol Oceanogr 45: 1067–1076.
Martiny AC, Kathuria S, Berube PM . (2009). Widespread metabolic potential for nitrite and nitrate assimilation among Prochlorococcus ecotypes. Proc Natl Acad Sci USA 106: 10787–10792.
Mason OU, Nakagawa T, Rosner M, Van Nostrand JD, Zhou J . (2010). First investigation of the microbiology of the deepest layer of ocean crust. PLoS One 5: e15399.
Mayer JA, Taylor FJR . (1979). Virus which lyses the marine nanoflagellate Micromonas pusilla. Nature 281: 299–301.
Mella-Flores D, Mazard S, Humily F, Partensky F, Mahé F, Bariat L et al (2011). Is the distribution of Prochlorococcus and Synechococcus ecotypes in the Mediterranean Sea affected by global warming. Biogeosciences 8: 2785–2804.
Milligan KLD, Cosper EM . (1994). Isolation of virus capable of lysing the brown tide microalga, Aureococcus anophagefferens. Science 266: 805–807.
Moisander PH, Beinart RA, Hewson I, White AE, Johnson KS, Carlson CA et al (2010). Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain. Science 327: 1512–1514.
Moisander PH, Morrison AE, Ward BB, Jenkins BD, Zehr JP . (2007). Spatial-temporal variability in diazotroph assemblages in Chesapeake Bay using an oligonucleotide nifH microarray. Environ Microbiol 9: 1823–1835.
Moisander PH, Shiue L, Steward GF, Jenkins BD, Bebout BM, Zehr JP . (2006). Application of a nifH oligonucleotide microarray for profiling diversity of N2-fixing microorganisms in marine microbial mats. Environ Microbiol 8: 1721–1735.
Moisander PH, Zhang R, Boyle EA, Hewson I, Montoya JP, Zehr JP . (2012). Analogous nutrient limitations in unicellular diazotrophs and Prochlorococcus in the South Pacific Ocean. ISME J 6: 733–744.
Moore JK, Donney SC, Lindsay K, Mahowald N, Michaels AF . (2006). Nitrogen fixation amplifies the ocean biogeochemical response to decadal timescale variations in mineral dust deposition. Tellus Ser B 58: 560–572.
Moore LR, Post AF, Rocap G, Chisholm SW . (2002). Utilization of different nitrogen sources by the marine cyanobacteria, Prochlorococcus and Synechococcus. Limnol Oceanogr 47: 989–996.
Mosier AC, Francis CA . (2011). Determining the distribution of marine and coastal ammonia-oxidizing archaea and bacteria using a quantitative approach. In: Klotz MG (ed) Methods in Enzymology: Research on Nitrification and Related Processes. Part A, vol. 486. Elsevier Academic Press: San Diego, CA, USA, pp 205–221.
Mulholland MR, Bronk D, Capone DG . (2004). Dinitrogen fixation and release of ammonium and dissolved organic nitrogen by Trichodesmium IMS101. Aquat Microb Ecol 37: 85–94.
Mulholland MR, Capone DG . (2001). Stoichiometry of nitrogen and carbon utilization in cultured populations of Trichodesmium IMS101: Implications for growth. Limnol Oceanogr 46: 436–443.
Neidhardt FC, Umbarger HE . (1996). Chemical composition of Escherichia coli. In: Neidhardt FC, Curtiss III R, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, et al (eds). Escherichia coli and Salmonella: Cellular and Molecular Biology 2nd edn. ASM Press: Washington, DC, USA, pp 13–16.
Orchard ED, Webb EA, Dyhrman S . (2009). Molecular analysis of the phosphorus starvation response in Trichodesmium spp. Environ Microbiol 11: 2400–2411.
Paerl RW, Johnson KS, Welsh RM, Worden AZ, Chavez FP, Zehr JP . (2011). Differential distributions of Synechococcus subgroups across the California Current System. Front Microbiol 2: 59.
Paerl RW, Turk KA, Beinart RA, Chavez FP, Zehr JP . (2012). Seasonal change in the abundance of Synechococcus and multiple distinct phylotypes in Monterey Bay determined by rbcL and narB quantitative PCR. Environ Microbiol 14: 580–593.
Palenik B, Ren QH, Dupont CL, Myers GS, Heidelberg JF, Badger JH et al (2006). Genome sequence of Synechococcus CC9311: Insights into adaptation to a coastal environment. Proc Natl Acad Sci USA 103: 13555–13559.
Post AF, Penno S, Zandbank K, Paytan A, Huse S, Mark Welch D . (2011). Long term seasonal dynamics of Synechococcus population structure in the Gulf of Aqaba, Northern Red Sea. Front Microbiol 2: 131.
Poulsen N, Kröger N . (2005). A new molecular tool for transgenic diatoms. FEBS J 272: 3413–3423.
Rhee SK, Liu XD, Wu LY, Chong SC, Wan XF, Zhou JZ . (2004). Detection of genes involved in biodegradation and biotransformation in microbial communities by using 50-mer oligonucleotide microarrays. Appl Environ Microbiol 70: 4303–4317.
Rich VI, Konstantinidis K, DeLong EF . (2008). Design and testing of ‘genome-proxy’ microarrays to profile marine microbial communities. Environ Microbiol 10: 506–521.
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.
Rinta-Kanto JM, Buergmann H, Gifford SM, Sun S, Sharma S, del Valle DA et al (2011). Analysis of sulfur-related transcription by Roseobacter communities using a taxon-specific functional gene microarray. Environ Microbiol 13: 453–467.
Scanlan DJ, Bourne JA, Mann NH . (1996). A putative transcriptional activator of the Crp/Fnr family from the marine cyanobacterium Synechococcus sp. WH7803. J Appl Phycol 8: 565–567.
Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, Hess WR et al (2009). Ecological genomics of marine picocyanobacteria. Microbiol Mol Bio Rev 73: 249–299.
Scanlan DJ, West NJ . (2002). Molecular ecology of the marine cyanobacterial genera. FEMS Microbiol Ecol 40: 1–12.
Sebastian M, Ammerman JW . (2009). The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. ISME J 3: 563–572.
Shi YM, Tyson GW, DeLong EF . (2009). Metatranscriptomics reveals unique microbial small RNAs in the ocean's water column. Nature 459: 266–269.
Singh AK, McIntyre LM, Sherman LA . (2003). Microarray analysis of the genome-wide response to iron deficiency and iron reconstitution in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 132: 1825–1839.
Smith MW, Herfort L, Tyrol K, Suciu D, Campbell V, Crump BC et al (2010). Seasonal changes in bacterial and archaeal gene expression patterns across salinity gradients in the Columbia River coastal margin. PLoS One 5: e13312.
Smyth GK . (2005). LIMMA: Linear Models for Microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W (eds) Bioinformatics and Computational Biology Solutions using R and Bioconductor. Springer: New York, NY, USA, pp 397–420.
Song BK, Ward BB . (2004). Molecular characterization of the assimilatory nitrate reductase gene and its expression in the marine green alga Dunaliella tertiolecta (Chlorophyceae). J Phycol 40: 721–731.
Stuart RK, Dupont CL, Johnson DA, Paulsen IT, Palenik B . (2009). Coastal strains of marine Synechococcus exhibit increased tolerance to copper shock and a distinctive transcriptional response relative to open ocean strains. Appl Environ Microbiol 75: 5047–5057.
Sun S, Chen J, Li W, Altinatas I, Lin A, Peltier S et al (2011). Community cyberinfrastructure for Advanced Microbial Ecology Research and Analysis: the CAMERA resource. Nucl Acids Res 39: D546–D551.
Sun J, Steindler L, Thrash JC, Halsey KH, Smith DP, Carter AE et al (2011). One carbon metabolism in SAR11 pelagic marine bacteria. PLoS One 6: e23973.
Sunda WG, Swift DG, Huntsman SA . (1991). Low iron requirement for growth in oceanic phytoplankton. Nature 351: 55–57.
Sylvan J, Quigg A, Tozzi S, Ammerman J . (2007). Eutrophication-induced phosphorus limitation in the Mississippi River plume: evidence from fast repetition rate fluorometry. Limnol Oceanogr 52: 2679–2685.
Sylvan JB, Quigg A, Tozzi S, Ammerman JW . (2011). Mapping phytoplankton community physiology on a river impacted continental shelf: testing a multifaceted approach. Estuaries Coasts 34: 1220–1233.
Taroncher-Oldenburg G, Griner EM, Francis CA, Ward BB . (2003). Oligonucleotide microarray for the study of functional gene diversity in the nitrogen cycle in the environment. Appl Environ Microbiol 69: 1159–1171.
Tetu SG, Brahamsha B, Johnson DA, Tai V, Phillippy K, Palenik B et al (2009). Microarray analysis of phosphate regulation in the marine cyanobacterium Synechococcus sp. WH8102. ISME J 3: 835–849.
Thompson AW, Huang K, Saito MA, Chisholm SW . (2011). Transcriptome response of high- and low-light-adapted Prochlorococcus strains to changing iron availability. ISME J 5: 1580–1594.
Tiquia SM, Wu L, Chong SC, Passovets S, Xu D, Xu Y et al (2004). Evaluation of 50-mer oligonucleotide arrays for detecting microbial populations in environmental samples. Biotechniques 36: 664–675.
Tolonen AC, Aach J, Lindell D, Johnson ZI, Rector T, Steen R et al (2006). Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability. Mol Syst Biol 2: 53.
Tusher VG, Tibshirani R, Chu G . (2001). Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116–5121.
Vogel J, Axmann IM, Herzel H, Hess WR . (2003). Experimental and computational analysis of transcriptional start sites in the cyanobacterium Prochlorococcus MED4. Nucleic Acids Res 31: 2890–2899.
Ward BB, Eveillard D, Kirshtein JD, Nelson JD, Voytek MA, Jackson GA . (2007). Ammonia-oxidizing bacterial community composition in estuarine and oceanic environments assessed using a functional gene microarray. Environ Microbiol 9: 2522–2538.
Watkins-Brandt KS, Letelier RM, Spitz YH, Church MJ, Böttjer D, White AE . (2011). Addition of inorganic or organic phosphorus enhances nitrogen and carbon fixation in the oligotrophic North Pacific. Mar Ecol Prog Ser 432: 17–29.
Wawrik B, Boling WB, Van Nostrand JD, Xie J, Zhou J, Bronk DA . (2012). Assimilatory nitrate utilization by bacteria on the West Florida Shelf as determined by stable isotope probing and functional microarray analysis. FEMS Microbiol Ecol 79: 400–411.
Webb EA, Moffett JW, Waterbury JB . (2001). Iron stress in open-ocean cyanobacteria (Synechococcus, Trichodesmium, and Crocosphaera spp.): identification of the IdiA protein. Appl Environ Microbiol 67: 5444–5452.
White AE, Spitz YH, Letelier RM . (2007). What factors are driving summer phyto-plankton blooms in the North Pacific Subtropical Gyre? J Geophys Res 112: C12006.
Wu L, Kellogg L, Devol AH, Tiedje JM, Zhou J . (2008). Microarray-based characterization of microbial community functional structure and heterogeneity in marine sediments from the Gulf of Mexico. Appl Environ Microbiol 74: 4516–4529.
Wu LY, Thompson DK, Li GS, Hurt RA, Tiedje JM, Zhou JZ . (2001). Development and evaluation of functional gene arrays for detection of selected genes in the environment. Appl Environ Microbiol 67: 5780–5790.
Xie J, He Z, Liu X, Liu X, Van Nostrand JD, Deng Y et al (2011). GeoChip-based analysis of the functional gene diversity and metabolic potential of microbial communities in acid mine drainage. Appl Environ Microbiol 2011: 3.
Yergeau E, Kang S, He Z, Zhou J, Kowalchuk GA . (2007). Functional microarray analysis of nitrogen and carbon cycling genes across an Antarctic latitudinal transect. ISME J 1: 163–179.
Zehr JP, Montoya JP, Jenkins BD, Hewson I, Mondragon E, Short CM et al (2007). Experiments linking nitrogenase gene expression to nitrogen fixation in the North Pacific subtropical gyre. Limnol Oceanogr 52: 169–183.
Zhou A, He Z, Qin Y, Lu Z, Deng Y, Tu Q et al (2013). StressChip as a high-throughput tool for assessing microbial community responses to environmental stresses. Environ Sci Technol 47: 9841–9849.
Acknowledgements
This work resulted from two workshops, and the design of the microarray was partially supported by the Gordon and Betty Moore Foundation (the MEGAMER facility), by a Gordon and Betty Moore Foundation Marine Investigator grant (JPZ) and by the NSF Center for Microbial Oceanography (C-MORE, NSF EF0424599). We thank all the participants of the October 2010 MicroTOOLs workshop sponsored by the Moore foundation. Particularly, we thank those who provided sequences for the design of microarray: Mahdi Belcaid, Dreux Chappell, Jackie Collier, Chris Francis, Scott Gifford, Jana Grote, Bethany Jenkins, Julie LaRoche, Pia Moisander, Annika Mosier, Micaela Parker, Holly Simon, Mariya Smit, Jody Wright, and Louie Wurch. We thank Shulei Sun and the team at CAMERA for support during microarray design. We also thank the Hawaii Ocean Time-series (HOT) program and C-MORE, specifically the captain and crew of R/V Kilo Moana and chief scientist of KM1016 cruise, Matt Church, for their expertise and for providing the opportunity and support for conducting experiments at sea. We thank Philip Heller and Jonathan Magasin for developing Java scripts for the microarray design and for computational support during the MicroTOOLs workshop in October 2010. Finally, we thank Nicole Pereira for help in running the incubation experiment, Sasha Tozzi for FRRF measurements, Rob Tibshirani for a consultation on microarray data normalization and analysis and the JPZ laboratory members for constructive discussions.
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Shilova, I., Robidart, J., James Tripp, H. et al. A microarray for assessing transcription from pelagic marine microbial taxa. ISME J 8, 1476–1491 (2014). https://doi.org/10.1038/ismej.2014.1
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