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or collective redistirbution other or collective or means this reposting, of machine, is by photocopy article only anypermitted of with portion the approvalOceanography S The of This article has been published in published been This has article A s e a o f M i c r e s

> Section V. Ex amples of Diversit y

> Chapter 10. Microbial Communities Oceanography > B. Polar Microbiology Microbiology in Polar , Volume 2, a quarterlyOceanography 20, Number S The journal of By Ja mes T. Hollibaugh, Connie Lovejoy, and Alison E. Murr ay

The Polar Oceans strains wind mixing and the land-locked basin receiving ~10% of the global run- Polar oceans are distinct from other geography of the basin restricts exchange off of freshwater (Aagaard and Carmack, oceanic environments in a number of with lower-latitude waters. Other char- 1989), while the Southern sur- ways, but the presence of ice is a acteristics of polar oceans, such as low rounds an ice-covered land mass and is major habitat difference. Sea ice affects temperature and intense seasonal varia- separated from lower-latitude waters by a polar microbial communities by limit- tion in primary production and carbon well-defined circumpolar front. The riv- ociety. CopyrightOceanography S 2007 by The ing light penetration into the upper flux, are often more extreme than in ers emptying into the Ocean drain ocean and by providing a unique sea- other oceanic habitats. lower-latitude terrestrial environments, surface habitat (Figures 1 and 2). Sea ice Unique differences between the two including and boreal forests. serves as a support matrix for a diverse polar oceans are due to the circumstance These rivers are quantitatively important and dynamic assemblage of microbes, that the is a land-locked sources of organic carbon to the Arctic including phytoplankton and pro- karyotes, often referred to as the sea-

ice microbial community, or SIMCO. ociety. A

Growth of ice-associated microalgae can ociety. S ll rights reserved. Permission is reserved. ll rights granted to in teaching copy this and research. for use article R lead to extreme carbon enrichment in end all correspondence to:Oceanography S [email protected] Th e or the ice, fueling microbial production and providing a food supply for herbivorous metazoa. Brine exclusion during the for- mation of sea ice, coupled with summer melting, contributes to significant and persistent water-column stratification. This is especially the case in the Arctic Ocean where permanent ice cover con-

James T. Hollibaugh (aquadoc@uga. edu) is Professor, Department of Marine ociety, 1931, R Box PO Sciences, University of Georgia, Athens, GA, USA. Connie Lovejoy is Professor, Department of Biology, Université Laval, ockville, M D 20849-1931, USA ockville, Québec, Canada. Alison E. Murray epublication, systemmatic reproduction, is Associate Research Professor, Desert Figure 1. This late-season sea ice is tinged brown from the growth of microorganisms and algae growing on the bottom and in the flooded pores of the disintegrating ice. Note the low ceiling and thick cloud Research Institute and Adjunct Professor, cover, fairly typical of polar oceans for much of the year and further reducing the light available to water- University of Nevada, Reno, NV, USA. column primary producers. Photo courtesy of Alison Murray .

140 Oceanography Vol. 20, No. 2 Ocean (Opsahl et al., 1999; Benner et al., Figure 2. Close-up of sea ice 2005). The receives no containing a thick microbial community. Photo courtesy of such terrestrial carbon subsidy. Alison Murray

Polynyas Limited areas of persistently open water provide habitats that contrast with areas that are ice covered during much of the year. These open-water areas, called , result from a variety of physi- cal processes. There have been several studies focusing on polynyas in recent years, notably the Canadian-led North Water (NOW) study (Deming et al., 2002). The NOW polynya was occupied for over four months in 1998, from April through July, and also sam- pled in the late summer and early fall of 1997 and 1999 (Figure 3). These stud- Max Dunbar in the 1960s. SIMCO are and can be found both free-living and ies show that microbes in the polynya rich communities of prokaryotic and attached to algal cells in the dense were more active than their counterparts eukaryotic organisms found in sea ice assemblages that form within the ice under the adjacent ice cover. There is at both poles. Brine channels that form (Palmisano and Garrison, 1993). Sea- little overlap between the phytoplank- as salts are excluded during the freezing ice-associated are more likely to ton found in adjacent sea ice process provide a major SIMCO habitat be true psychrophiles (optimal growth and open waters and the distinct phyto- within the ice. Sea-ice brines are reser- temperatures < 15°C) (Delille, 1992) plankton communities associated with voirs of dissolved organic and inorganic than their planktonic counterparts, different water masses that meet in the nutrients, and are home to abundant and produce more colony-forming NOW (Lovejoy et al., 2002a, 2002b). bacterial populations. The diversity and units (CFU) per volume sampled than Work in the NOW in 2005 using clone ecology of SIMCO bacteria have been populations (Bowman et al., library analysis shows that the bacte- the subjects of numerous studies over 1997a; Brinkmeyer et al., 2003; Junge et rial and archaeal communities found the years, with recent efforts focusing on al., 2002). Molecular taxonomic char- in open waters are more similar to describing the phylogenetic composi- acterization of sea-ice bacterial diver- other open oceans than to the special- tion of bacterial assemblages. Archaeal sity using 16S rRNA gene sequencing ized sea-ice communities (recent work populations have not been characterized suggests that although there are some of author Lovejoy and Pierre Galand, as thoroughly, though they have been organisms in common between the sea Université Laval). detected in SIMCO in at least one study ice and underlying seawater, many of (Junge et al., 2004). the psychrophilic species appear to be Sea-Ice Assemblages Bacteria were first observed in unique to the sea-ice habitat (Bowman, Sea-ice microbial communities have sea ice in 1966 (Iizuka et 1997b). Most SIMCO bacteria are affili- been the focus of polar investigations al., 1966). SIMCO bacteria are often ated with the (alpha- and for many years, with some of the early reported to be larger than pelagic gamma-Proteobacteria), Bacteriodetes, characterizations going back to the forms, are capable of rapid growth and Actinobacteria phyla. The question work of John Bunt, Rita Horner, and rates (Kottmeier and Sullivan, 1987), of marine microbial biogeography was

Oceanography June 2007 141 from electron microscopy examinations of polar ocean samples. With additional environmental rRNA sequence data now available from many oceanic , it is becoming feasible to distinguish biogeographies of these uncultivated eukaryotic microbes. For example, Massana et al. (2006) found that the among 12 MAST subclades, at least one (MAST 4) is absent from polar waters, and Lovejoy et al. (2007) recently described a polar ecotype of the small prasinophyte Micromonas with pan- Arctic distribution. This 1–2 µm cell is ubiquitous throughout the Arctic basin Figure 3. Ice-covered oceans present a special challenge for sampling, as well as unique environmental conditions. Here, the Canadian icebreaker Radisson occupies a station during the North Water Polynya and, as the persistent dominant of the study. Photo courtesy of Connie Lovejoy deep chlorophyll maximum layer, is a major contributor to primary produc- tion in the Arctic Ocean. The physi- first introduced and examined by study- uncovered three major new clades of ological adaptation of this ecotype to ing gas vacuolate psychrophiles isolated marine eukaryotes: group I and II alveo- low temperatures and light may well be from both poles (Staley and Gosink, lates and marine stramenopiles (MAST) widespread among polar protists. 1999). Gas vacuolate bacteria are postu- that have since been reported from lated to be adapted to a SIMCO lifestyle throughout the world’s and ocean. Bacterioplankton because their buoyancy would ensure The largest survey of picoeukaryotes in Bacterioplankton, including organisms inclusion in forming sea ice. Commonly the Arctic to date reports that 42% of in the domains Bacteria and Archaea, isolated gamma-Proteobacteria phy- the sequences retrieved are less than dominate the picoplankton in both the lotypes from both poles fall into the 98% identical to sequences from other Arctic and Southern Oceans. The func- genera Glaciecola, Psychrobacter, and oceanographic regions (Lovejoy et al., tion of these organisms in polar oceans Colwellia; the alpha-Proteobacteria 2006). Two clades of small radiolar- is similar to their function in lower into the genera Octadecabacter and ians within the family Spongodiscidae latitudes: to grow, heterotrophs and Sulfitobacter; and Bacteriodetes into the and class Polycystinea found among photo-heterotrophs use organic car- genera Polaribacter, Flavobacterium, and these sequences had closest matches to bon produced by phytoplankton and Psychroserpens. (Brown and Bowman, Antarctic sequences. This could indicate sea-ice algae. Chemolithoautotrophic 2001; Junge et al., 2002). bipolar distribution of these organisms bacteria appear to be widespread in and their importance in polar waters. polar oceans and to mediate inorganic Picoeukaryotes That study also revealed at least one nitrogen (Hollibaugh et al., 2002) and López-Garcia et al. (2001a, 2001b) pro- clade of heterokont algae (a major line sulfur transformations. Secondary pro- vided one of the first reports of novel, of eukaryotes) that was distinct from duction rates in polar waters during uncultivated picoeukaryotes in the open either diatoms or bolidophytes. Lovejoy summer are similar to those in lower ocean from samples collected in deep et al. (2006) speculate that the sequences latitudes, despite much colder ocean waters of the Antarctic polar front. Their could be candidates for the polar temperatures (Fuhrman and Azam, analysis of an 18S rRNA clone library Parmales, a group of algae known only 1980; Hollibaugh et al., 1992). Winter

142 Oceanography Vol. 20, No. 2 rates are much lower, however, likely due on cultivated organisms. Recent reports but more details can be found in reviews to carbon limitation. Bacterioplankton of studies in Bay (Maugeri such as Murray and Grzymski (2007) for blooms have been detected in the sub- et al., 1996; Michaud et al., 2004) and the Antarctic and Bano and Hollibaugh Antarctic (Delille et al., 1996) and in the McMurdo Sound (Webster et al., 2004) (2002) for the Arctic. during late summer (February) reported high diversity, while another Psychrophilic marine bacteria are phe- (Ducklow et al., 2001), lagging, rather study comparing strains isolated from notypically and genotypically divergent than being directly coupled to, seasonal both poles (Mergaert et al., 2001) reports in comparison to their mesophilic rela- spring phytoplankton blooms as they are that five of eight clusters derived using tives. Psychrophile genomes may contain at lower latitudes. In addition to strong numerical were common specific genes that facilitate cold adapta- seasonal dynamics in bacterioplankton to both poles. Diversity studies of the tion, such as the nucleic-acid-binding abundance and activity, bacterial spe- 16S rRNA gene sequence provide similar proteins found in methanogenic archaea cies composition in coastal Antarctic findings in which polar species (from from an Antarctic lake (Saunders et al., Peninsula waters shifts. Phylogenetic either pole) are the nearest relatives 2003), though the current paradigm is analyses based on 16S rRNA genes sug- (Murray and Grzymski, 2007). that highly active enzymes are strongly gest over 50% turnover in community Many cosmopolitan marine groups selected and have undergone significant composition between winter and sum- have been detected in waters from modifications in amino-acid usage (Feller mer (Murray and Grzymski, 2007; both poles. Organisms in the SAR86 and Gerday, 2003). With the recent Murray et al., 1998). Hodges et al. (2005) (Béjà et al., 2002), SAR11 (Mullins completion of several genome sequences, and Yager et al. (2001) report similar sea- et al., 1995; Giovannoni et al., 2005), themes in cold adaptation are becoming sonal shifts in the Arctic Ocean. and Flavobacteria groups (Gómez- more evident. Adaptation to permanently Similar groups of bacterioplankton Consarnau et al., 2007) are found in cold conditions has been investigated inhabit polar seas and lower-latitude both Arctic (Bano and Hollibaugh, 2002) through analysis of amino-acid usage waters, with dominance of organisms and Antarctic (Murray and Grzymski, in bacterial genomes. Adaptations pre- related to alpha-Proteobacteria, gamma- 2007) samples, suggesting the impor- sumed to increase cold tolerance, such as Proteobacteria, Actinobacteria, and tance of these organisms in these eco- a reduction in charged amino-acid resi- Bacteriodetes (Bano and Hollibaugh, systems. Members of these groups are dues forming salt bridges, a bias towards 2002; Bowman et al., 1997b; Murray and known to produce proteorhodopsin asparagine residues, and a reduction in Grzymski, 2007). Though comprehensive studies comparing the levels of diversity in polar waters to other oceanic systems sea ice affects polar microbial communities by have not been conducted, it appears that they are comparable. The most limiting light penetration into the upper ocean notable difference is the lack of cyano- and by providing a unique sea-surface habitat bacteria (especially Prochlorococcus) in polar waters (Letelier and Karl, 1989; Zubkov et al., 1998; Johnson et al., and thus they may benefit from energy proline and hydrophobic clusters, have 2006). Garneau et al. (2006) detected obtained from proteorhodopsin-proton been reported (Grzymski et al., 2006; Synechococcus in Arctic waters; however, pumping actions. Aerobic anoxygenic Medigue et al., 2005; Methe et al., 2005). they are related to freshwater clades and phototrophs related to the Roseobacter their occurrence seems to be the result of clade also appear to be abundant in Archaeoplankton freshwater input (Waleron et al., 2007). both polar coastal and oceanic systems Planktonic archaea in polar waters Most research concerning the diversity (Selje et al., 2004). A detailed descrip- appear to be dominated by the marine of polar marine bacteria has focused tion is beyond the scope of this article, Group I Crenarchaeota (Bano et al.,

Oceanography June 2007 143 2004; Church et al., 2003; DeLong et tially sequenced by Béjà et al. (2002) Brown, M.V., and J.P. Bowman. 2001. A molecular phylogenetic survey of sea-ice microbial com- al., 1994; Galand et al., 2006; Massana suggest a lack of synteny (preservation munities (SIMCO). FEMS Microbiology Ecology et al., 1998; Murray et al., 1998; Wells of gene order between related species), 35:267–275. Church, M.J., E.F. DeLong, H.W. Ducklow, M.B. et al., 2006; Wells and Deming, 2003). indicating genomic complexity beyond Karner, C.M. Preston, and D.M. Karl. 2003. Group II marine Euryarchaeota have that seen in the 16S rRNA gene sequence Abundance and distribution of planktonic Archaea and Bacteria in the waters west of the also been detected (DeLong et al., 1994), of the marine Group I Crenarchaeota. . Limnology and Oceanography as have GIII and GIV Crenarchaeota 48:1,893–1,902. Delille, D. 1992. Marine bacterioplankton at the in the deep polar frontal waters of the Acknowledgements ice edge, distribution of psychrophilic Antarctic (López-Garcia et al., 2004) JTH’s contribution was supported and psychrotrophic populations. Polar Biology 12:205–210 and in Arctic waters (Bano et al., 2004; by NSF OPP-0234249. CL is grate- Delille, D., L. Mallard, and C. Rosiers. 1996. Inter- Galand et al., 2006). The marine Group I ful for support from Natural Sciences annual variability in marine coastal Antarctic bac- terioplankton. Polar Biology 16:19–25. Crenarchaeota are unique in their dis- and Engineering Research Council of DeLong, E.F., K.Y. Wu, B.B. Prezelin, and R.V.M. tribution as they have been detected Canada (NSERC), and Fonds Québécois Jovine. 1994. High abundance of Archaea in Antarctic marine picoplankton. Nature in winter surface waters in high rela- de Recherche sur la Nature et les 371:695–697. tive abundance (~ 20% of total rRNA) Technologies (FQRNT). AEM was sup- Deming, J.W., L. Fortier, and M. Fukuchi. 2002. The International North Water Polynya Study (NOW): in comparison to other lower-latitude ported in part by OPP-0085435. A brief overview. Deep-Sea Research Part II waters where they are rarely detected 49:4,887–4,892. Ducklow, H.W., C.A. Carlson, M. Church, D. in surface waters (Murray et al., 1998). References Kirchman, D. Smith, and G. Steward. 2001. The seasonal development of the bacterioplankton They are abundant in deeper polar Aagaard, K., and E.C. Carmack. 1989. The role of sea ice and other fresh water in the Arctic circulation. bloom in the Ross Sea, , 1994–1997. waters as in other regions of the ocean Journal of Geophysical Research 94:14,485–14,498. Deep-Sea Research Part II 48:4,199–4,221. Feller, G., and C. Gerday. 2003. Psychropilic enzymes: (Church et al., 2003; Karner et al., 2001). Bano, N., and J.T. Hollibaugh. 2002. Phylogenetic Composition of Bacterioplankton Assemblages Hot topics in cold adaptation. Nature Reviews Activities of these archaea remain to be from the Arctic Ocean. Applied and Environmental Microbiology 1:200–208. Francis, C.A., K.J. Roberts, J.M. Beman, A.E. Santoro, demonstrated in polar waters, though Microbiology 68:505–518. Bano, N., S. Ruffin, B. Ransom, and J.T. Hollibaugh. and B.B. Oakley. 2005. Ubiquity and diversity of some of them may play roles as ammo- 2004. Phylogenetic composition of Arctic Ocean ammonia-oxidizing archaea in water columns and archaeal assemblages and comparison with ant- sediments of the ocean. Proceedings of the National nia oxidizers, as has been suggested for arctic assemblages. Applied and Environmental Academy of Sciences of the United States of America other Crenarchaeota affiliated with this Microbiology 70:781–789. 102:14,683–14,688. Béjà, O., E.V. Koonin, L. Aravind, L.T. Taylor, H. Frigaard, N.U., A. Martinez, T.J. Mincer, and E.F. lineage (Francis et al., 2005; Konneke et Seitz, J.L. Stein, D.C. Bensen, R.A. Feldman, R.V. DeLong. 2006. Proteorhodopsin lateral gene al., 2005). In addition, a relative of the Swanson, and E.F. DeLong. 2002. Comparative transfer between marine planktonic Bacteria and genomic analysis of archaeal genotypic variants in Archaea. Nature 439:847–850. Group II Euryarchaeota is reported to a single population and in two different oceanic Fuhrman, J.A., and F. Azam. 1980. Bacterioplankton contain a proteorhodopsin ortholog, provinces. Applied and Environmental Microbiology secondary production estimates for coastal waters 68:335–345. of British Columbia, Antarctica, and California. suggesting that this group of archaea, Benner, R., P. Louchouarn, and R. M. W. Amon. 2005. Applied and Environmental Microbiology whose distribution is mostly restricted to Terrigenous dissolved organic matter in the Arctic 39:1,085–1,095. Ocean and its transport to surface and deep waters Galand, P.E., C. Lovejoy, and W.F. Vincent. 2006. surface waters, can use the light-driven of the North Atlantic, Global Biogeochemical Cycles, Remarkably diverse and contrasting archaeal rhodopsin proton pump to generate 19, GB2025, doi:10.1029/2004GB002398 communities in a large arctic river and the Bowman, J.P., M.V. Brown, and D.S. Nichols. 1997a. coastal Arctic Ocean. Aquatic Microbial Ecology a proton motive force (Frigaard et al., Biodiversity and ecophysiology of bacteria asso- 44:115–126. 2006). Marine archaea have not been ciated with . Antarctic Science Garneau, M.E., W.F. Vincent, L. Alonso-Saez, Y. 9:134–142. Gratton, and C. Lovejoy. 2006. Prokaryotic com- cultivated from the poles; thus, knowl- Bowman, J.P., S.A. McCammon, M.V. Brown, D.S. munity structure and heterotrophic production in edge of this domain has been solely Nichols, and T. A. McMeekin. 1997b. Diversity and a river-influenced coastal arctic ecosystem. Aquatic association of psychrophilic bacteria in Antarctic Microbial Ecology 42:27–40. through environmental molecular sur- sea ice. Applied and Environmental Microbiology Giovannoni, S.J., H.J. Tripp, S. Givan, M. Podar, veys, fluorescent in situ hybridization 63:3,068–3,078. K.L. Vergin, D. Baptista, L. Bibbs, J. Eads, T.H. Brinkmeyer, R., K. Knittel, J. Jurgens, H. Weyland, Richardson, M. Noordewier, and others. 2005. studies, and environmental genomic R. Amann, and E. Helmke. 2003. Diversity and Genome streamlining in a cosmopolitan oceanic structure of bacterial communities in arctic ver- sequencing (Béjà et al., 2002). Several bacterium. Science 309:1,242–1,245. sus antarctic pack ice. Applied and Environmental Gómez-Consarnau, L., J.M. González, M. Coll-Lladó, genomic fragments identified and par- Microbiology 69:6,610–6,619. P. Gourdon, T. Pascher, R. Neutze, C. Pedrós-Alió,

144 Oceanography Vol. 20, No. 2 and J. Pinhassi. 2007. Light stimulates growth of López-Garcia, P., C. Brochier, D. Moreira, and F. Murray, A.E., and J.J. Grzymski. 2007. Genomics and proteorhodopsin-containing marine Flavobacteria. Rodríguez-Valera. 2004. Comparative analysis of a diversity of Antarctic marine microorganisms. Nature 445:210–213. genome fragment of an uncultivated mesopelagic Philosophical Transactions of the Royal Society B. Grzymski, J.J., B.J. Carter, E.F. DeLong, R.A. Feldman, crenarchaeote reveals multiple horizontal gene 362, doi: 10.1098/rstb.2006.1944. A. Ghadiri, and A.E. Murray. 2006. Comparative transfers. Environmental Microbiology 6:19-34. Murray, A.E., C.M. Preston, R. Massana, L.T. Taylor, genomics of DNA fragments from six antarc- Lovejoy, C., L. Legendre, M.-J. Martineau, J. Bâcle, and A. Blakis, K. Wu, and E.F. DeLong. 1998. Seasonal tic marine planktonic bacteria. Applied and C.H. von Quillfeldt. 2002a. Distribution of phy- and spatial variability of bacterial and archaeal Environmental Microbiology 72:1,532–1,541. toplankton and other protists in the North Water. assemblages in the coastal waters off Anvers Hodges, L.R., N. Bano, J.T. Hollibaugh, and P.L. Yager. Deep-Sea Research Part II 49:5,027–5,047 Island, Antarctica. Applied and Environmental 2005. Variation of bacterioplankton richness and Lovejoy, C., E.C. Carmack, L. Legendre, and N.M. Microbiology 64:2,585–2,595. similarity in areas of high and low particle concen- Price. 2002b. Water column interleaving: A new Opsahl, S., R. Benner, and R.M.W. Amon. 1999. tration in the arctic . Aquatic Microbial physical mechanism determining protist com- Major flux of terrigenous dissolved organic mat- Ecology 40:217–227. munities and bacterial states Limnology and ter through the Arctic Ocean. Limnology and Hollibaugh, J.T., N. Bano, and H.W. Ducklow. 2002. Oceanography 47:1,819–1,831. Oceanography 44:2,017–2,023 Widespread distribution in polar oceans of a 16S Lovejoy, C., R. Massana, and C. Pédros-Alió. 2006. Palmisano, A.C., and D.L. Garrison. Microorganisms rRNA gene sequence with affinity to Nitrosospira- Diversity and distribution of marine microbial in Antarctic sea ice. 1993. Pp. 167–218 in like ammonia-oxidizing bacteria. Applied and eukaryotes in the Arctic Ocean and adjacent Antarctic Microbiology. E. Imre Friedmann, ed., Environmental Microbiology 68:1,478–1,484. seas. Applied and Environmental Microbiology 72: Wiley-Liss, New York. Hollibaugh, J.T., P.S. Wong, F. Azam, D.C. Smith, G.F. 3,085–3,095. Saunders, N.F.W., T. Thomas, P.M.G. Curmi, J.S. Steward, and B.E. Cole. 1992. Measurement of Lovejoy, C., W.F. Vincent, S. Bonilla, S. Roy, M.J. Mattick, E. Kuczek, R. Slade, J. Davis, P.D. bacterioplankton production in Antarctic coastal Marineau, R. Terrado, M. Potvin, R. Massana, and Franzmann, D. Boone, K. Rusterholtz, and others. waters: Comparison of thymidine and L-leucine C. Pedrós-Alió. 2007. Distribution, phylogeny, and 2003. Mechanisms of thermal adaptation revealed methods and verification of labeling patterns. growth of cold-adapted picoprasinophytes in arctic from the genomes of the Antarctic Archaea Antarctic Journal of the United States 27:127–128. seas. Journal of Phycology 43:78–89. Methanogenium frigidum and Methanococcoides Iizuka, H., I. Tanabe, and H. Meguro. 1966. Massana, R., L.T. Taylor, A.E. Murray, K.Y. Wu, W.H. burtonii. Genome Research 13:1,580–1,588. Microorganisms in -ice of the Antarctic Jeffrey, and E.F. DeLong. 1998. Distribution of Selje, N., M. Simon, and T. Brinkhoff. 2004. A newly Ocean. Journal of General and Applied Microbiology marine planktonic archaea in the Gerlache strait, discovered Roseobacter cluster in temperate and 12:101–102. Antarctic Peninsula, during early spring. Limnology polar oceans. Nature 427:445–448. Johnson, Z.I., E.R. Zinser, A. Coe, N.P. McNulty, E.M.S. and Oceanography 43:607–617. Staley, J.T., and J.J. Gosink. 1999. Poles apart: Woodward, and S.W. Chisholm. 2006. Niche par- Massana, R., R. Terrado, I. Forn, C. Lovejoy, and C. Biodiversity and biogeography of sea ice bacteria. titioning among Prochlorococcus ecotypes along Pédros-Alió. 2006. Distribution and abundance of Annual Review of Microbiology 53:189–215. ocean-scale environmental gradients. Science uncultured heterotrophic flagellates in the world Waleron, M., K. Waleron, W.F. Vincent, and A. 311:1,737–1,740. oceans. Environmental Microbiology 8:1,515–1,522. Wilmotte. 2007. Allochthonous inputs of riverine Junge, K., H. Eicken, and J. W. Deming. 2004. Bacterial Maugeri, T.L., C. Gugliandolo, and V. Bruni. 1996. picocyanobacteria to coastal waters in the Arctic activity at-2 to-20 degrees C in Arctic wintertime Heterotrophic bacteria in the Ross Sea (Terra Nova Ocean. FEMS Microbial Ecology 59:356–365, doi: sea ice. Applied and Environmental Microbiology Bay, Antarctica). Microbiologica 19:67–76. 10.1111/j.1574-6941.2006.00236.x 70: 550–557. Medigue, C., E. Krin, G. Pascal, V. Barbe, A. Bernsel, Webster, N.S., A.P. Negri, M. Munro, and C.N. Junge, K., F. Imhoff, T. Staley, and J.W. Deming. 2002. P.N. Bertin, F. Cheung, S. Cruveiller, S. D’Amico, Battershill. 2004. Diverse microbial communi- Phylogenetic diversity of numerically important A. Duilio, and others. 2005. Coping with cold: The ties inhabit Antarctic sponges. Environmental arctic sea-ice bacteria cultured at subzero tempera- genome of the versatile marine Antarctica bacte- Microbiology 6:288–300. ture. Microbial Ecology 43:315–328. rium Pseudoalteromonas haloplanktis TAC125. Wells, L.E., M. Cordray, S. Bowerman, L.A. Miller, W.F. Karner, M.B., E.F. DeLong, and D.M. Karl. 2001. Genome Research 15:1,325–1,335. Vincent, and J.W. Deming. 2006. Archaea in par- Archaeal dominance in the mesopelagic zone of Mergaert, J., A. Verhelst, M.C. Cnockaert, T.-L. Tan, ticle-rich waters of the Beaufort Shelf and Franklin the . Nature 409:507–510. and J. Swings. 2001. Characterization of facultative Bay, Canadian Arctic: Clues to an allochthonous Konneke, M., A.E. Bernhard, J.R. De La Torre, C.B. oligotrophic bacteria from polar seas by analy- origin? Limnology And Oceanography 51:47–59. Walker, J.B. Waterbury, and D.A. Stahl. 2005. sis of their fatty acids and 16S rDNA sequences. Wells, L.E., and J.W. Deming. 2003. Abundance of Isolation of an autotrophic ammonia-oxidizing Systematic and Applied Microbiology 24:98–107. Bacteria, the Cytophaga-Flavobacterium cluster marine archaeon. Nature 437:543–546. Methe, B.A., K.E. Nelson, J.W. Deming, B. Momen, and Archaea in cold oligotrophic waters and neph- Kottmeier, S.T., and C.W. Sullivan. 1987. Late winter E. Melamud, X. Zhang, J. Moult, R. Madupu, eloid layers of the Northwest Passage, Canadian primary production and bacterial production in W.C. Nelson, R.J. Dodson, and others. 2005. The Archipelago. Aquatic Microbial Ecology 31:19–31. sea ice and seawater west of Antarctic Peninsula. psychrophilic lifestyle as revealed by the genome Yager, P.L., T.L. Connelly, B. Mortazavi, K.E. Marine Ecology Progress Series 36:287–298. sequence of Colwellia psychrerythraea 34H through Wommack, J. Bauer, S. Opsahl, J.T. Hollibaugh, Letelier, R.M., and D.M. Karl. 1989. Phycoerythrin- genomic and proteomic analyses. Proceedings of the and N. Bano. 2001. Dynamic bacterial and viral containing cyanobacteria in surface waters of the National Academy of Sciences of the United States of response to an algal bloom at sub-zero tempera- Drake Passage. Antarctic Journal of the United States America 102:10,913–10,918. tures. Limnology and Oceanography 46:790–801. 24:185–188. Michaud, L., F.D. Cello, M. Brilli, R. Fani, A.L. Guidice, Zubkov, M.V., M.A. Sleigh, G.A. Tarran, P.H. Burkill, López-Garcia, P., A. López-López, D. Moreira, and and V. Bruni. 2004. Biodiversity of cultivable and R.J.G. Leakey. 1998. Picoplanktonic commu- F. Rodríguez-Valera. 2001a. Diversity of free- psychrotrophic marine bacteria isolated from nity structure on an Atlantic transect from 50°N to living prokaryotes from a deep-sea site at the (Ross Sea, Antarctica). FEMS 50°S. Deep-Sea Research Part I 45:1,339–1,355. Antarctic polar front. FEMS Microbiology Ecology Microbiology Letters 230:63–71. 36:193–202. Mullins, T.D., T.B. Britschgi, R.L. Krest, and S.J. López-Garcia, P., F. Rodríguez-Valera, C. Pedrós-Alió, Giovannoni. 1995. Genetic comparisons reveal the and D. Moreira. 2001b. Unexpected diversity of same unknown bacterial lineages in Atlantic and small eukaryotes in deep-sea Antarctic plankton. Pacific bacterioplankton communities. Limnology Nature 409:603–607. and Oceanography 40:148–158.

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