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Biogeographic Partitioning of Southern Ocean Formicroorganisms Peer Review Revealed by Metagenomics Only Biogeographic partitioning of Southern Ocean Formicroorganisms Peer Review revealed by metagenomics Only Journal: Environmental Microbiology and Environmental Microbiology Reports Manuscript ID: EMI-2012-1032.R1 Manuscript Type: EMI - Research article Journal: Environmental Microbiology Date Submitted by the Author: n/a Complete List of Authors: Cavicchioli, Ricardo ecophysiology, element cycles and biogeochemical processes, environmental genomics, genomics/functional genomics/comparative Keywords: genomics, metagenomics/community genomics, microbial ecology, bacteria, archaea Wiley-Blackwell and Society for Applied Microbiology Page 1 of 848 1 Biogeographic partitioning of Southern Ocean microorganisms 2 revealed by metagenomics 3 4 David Wilkins 1, Federico M. Lauro 1, Timothy J. Williams 1, Matthew Z. Demaere 1, Mark 5 V. Brown 1,2 , JeffreyFor M. HoffmanPeer3, Cynthia Review Andrews-Pfannkoch Only3, Jeffrey B. Mcquaid 3, 6 Martin J. Riddle 4, Stephen R. Rintoul 5, Ricardo Cavicchioli 1,* 7 8 1 School of Biotechnology and Biomolecular Sciences, The University of New South Wales, 9 Sydney, New South Wales, 2052, Australia. 10 2 Evolution and Ecology Research Centre, The University of New South Wales, Sydney, New 11 South Wales, 2052, Australia. 12 3 J. Craig Venter Institute, 9704 Medical Center Drive, Rockville, MD, 20850, USA. 13 4 Australian Antarctic Division, Channel Highway, Kingston, Tasmania, 7050, Australia. 14 5 CSIRO Marine and Atmospheric Research, and Centre for Australian Weather and Climate 15 Research - A partnership of the Bureau of Meteorology and CSIRO, and CSIRO Wealth from 16 Oceans National Research Flagship, and the Antarctic Climate and Ecosystems Cooperative 17 Research Centre, Castray Esplanade, Hobart, Tas, 7001, Australia. 18 * To whom correspondence should be addressed: Ricardo Cavicchioli, School of Biotechnology 19 and Biomolecular Sciences, The University of New South Wales, Sydney, NSW, 2052, Tel. (+61 20 2) 9385 3516, Fax. (+61 2) 9385 2742, E-mail. [email protected] 21 22 Running title: Biogeography of Southern Ocean microorganisms 1 Wiley-Blackwell and Society for Applied Microbiology Page 2 of 848 23 Summary 24 We performed a metagenomic survey (6.6 Gbp of 454 sequence data) of Southern Ocean 25 (SO) microorganisms during the austral summer of 2007–2008, examining the genomic 26 signatures of communities across a latitudinal transect from Hobart (44°S) to the Mertz 27 Glacier, AntarcticaFor (67°S). Peer Operational Review taxonomic units (OTUs) Only of the SAR11 and SAR116 28 clades and the cyanobacterial genera Prochlorococcus and Synechococcus were strongly 29 overrepresented north of the Polar Front (PF). Conversely, OTUs of the 30 Gammaproteobacterial Sulfur Oxidizer-EOSA-1 (GSO-EOSA-1) complex, the phyla 31 Bacteroidetes and Verrucomicrobia and order Rhodobacterales were characteristic of 32 waters south of the PF. Functions enriched south of the PF included a range of 33 transporters, sulphur reduction and histidine degradation to glutamate, while branched- 34 chain amino acid transport, nucleic acid biosynthesis and methionine salvage were 35 overrepresented north of the PF. The taxonomic and functional characteristics suggested a 36 shift of primary production from cyanobacteria in the north to eukaryotic phytoplankton 37 in the south, and reflected the different trophic statuses of the two regions. The study 38 provides a new level of understanding about SO microbial communities, describing the 39 contrasting taxonomic and functional characteristics of microbial assemblages either side 40 of the PF. 41 42 Introduction 43 44 The SO plays a critical role in sustaining marine life around the globe. Upwelling of nutrient-rich 45 Circumpolar Deep Water (CDW) returns nutrients transported to the deep ocean by the sinking 2 Wiley-Blackwell and Society for Applied Microbiology Page 3 of 848 46 of organic matter (Rath et al. , 1998) and supports 75% of global ocean primary production north 47 of 30°S. Surface waters at high southern latitudes remain cold (< 3°C) year-round but undergo 48 extreme seasonal variations in sea-ice cover, light levels and day length. Primary production and 49 biomass are high in summer and very low in winter. Bacteria are abundant in the SO despite the 50 low temperaturesFor and seasonal Peer variability Review in productivity and are Only a major route for carbon flow 51 (Hessen et al. , 2004). 52 The SO is composed of several zones separated by circumpolar fronts, the locations of 53 which vary temporally and with longitude (Whitworth III, 1980; Orsi et al. , 1995; Sokolov and 54 Rintoul, 2002). The fronts separate regions with different physiochemical properties, such as 55 density, salinity, temperature and nutrient concentrations (Sokolov and Rintoul, 2002). 56 Hydrographic, bathythermographic and satellite altimetry data have been used to determine the 57 frontal structure of the Antarctic Circumpolar Current (ACC) south of Australia (Sokolov and 58 Rintoul, 2002). From north to south, the major fronts are the Subtropical Front (STF), the 59 Subantarctic Front (SAF), the Polar Front (PF) and the southern ACC front (SACCF). Each of 60 these fronts consists of multiple branches (Sokolov and Rintoul, 2002; Sokolov and Rintoul, 61 2009a, b). The Subantarctic Zone (SAZ) lies between the STF and SAF, the Polar Frontal Zone 62 (PFZ) lies between the SAF and the PF, and the Antarctic Zone (AZ) lies between the PF and the 63 Antarctic continent. 64 The PF has been suggested to be a major biogeographical boundary in the distribution and 65 abundance of both zooplankton (Chiba et al. , 2001; Hunt et al. , 2001; Esper and Zonneveld, 66 2002; Ward et al. , 2003) and bacterioplankton (Selje et al. , 2004; Abell and Bowman, 2005; 67 Giebel et al. , 2009; Weber and Deutsch, 2010). However, the microbial assemblages that 68 characterize Antarctic waters are generally poorly understood, and their diversity and functional 3 Wiley-Blackwell and Society for Applied Microbiology Page 4 of 848 69 capacity are not well characterized (Murray and Grzymski, 2007; Wilkins et al., 2012). Large 70 scale metagenome surveys have not previously been performed. 71 Recent anthropogenic climate change may be driving the warming and freshening of the 72 ACC (Boning et al. , 2008) and shifting it and its fronts poleward (Fyfe and Saenko, 2005; 73 Biastoch et al. ,For 2009). A community-levelPeer Review understanding is require Onlyd to effectively understand the 74 main components and dynamics of the microbial food web in the SO and thereby predict the 75 effects of a shifting ACC on the distribution and abundance of plankton. The oceanic changes 76 may have global ecological significance as the SO performs many ecosystem functions, 77 including significant sequestration of anthropogenic CO 2 (Sabine et al. , 2004; Mikaloff Fletcher 78 et al. , 2006) through both physiochemical processes and the “biological pump” of CO 2 fixation 79 (Thomalla et al. , 2011). 80 In the austral summer of 2006 we initiated a metagenome program based on the sampling 81 design of the Global Ocean Sampling (GOS) expedition (Rusch et al. , 2007), aimed at providing 82 a baseline to monitor microbial communities in the Australian section of the SO. To date we 83 have sampled SO water from 73° E to 150° E and 44° S to 68° S at depths from the surface to ~ 84 3700 m. In this study, we present data for plankton assemblages passed through a 20 µm prefilter 85 and captured onto sequential 0.1 µm, 0.8 µm and 3.0 µm filters. This fractionation approach was 86 originally adopted by the GOS expedition (Rusch et al. , 2007) and enables deeper sequencing of 87 a greater representation of the marine microbial community thereby improving the identification 88 of low-abundance taxa. By adopting this approach the metagenome datasets generated from the 89 SO can be directly compared to available GOS data (e.g. Brown et al.,2012). In studies of the SO 90 and marine derived Antarctic lakes, the approach has also proven useful for learning about the 91 microbial ecosystem in the context of resource partitioning, including particle attachment, 4 Wiley-Blackwell and Society for Applied Microbiology Page 5 of 848 92 trophic status and virus–host interactions (Ng et al. , 2010; Lauro et al. , 2011; Yau et al. , 2011; 93 Williams et al. , 2012b). 94 The samples in our SO study were collected in summer 2007/2008 on the SR3 transect 95 (Sokolov and Rintoul, 2002) of the Climate of Antarctica and the Southern Ocean (CASO), and 96 Collaborative EastFor Antarctica Peer Marine Census Review (CEAMARC) projects Only during the International 97 Polar Year (IPY) program (Fig.1). We assessed the taxonomic and functional profiles of 98 microbial communities from either side of the PF, thereby contributing important new 99 information about the microbial ecology of the SO and defining the microbial communities most 100 influenced by the effects of the PF forming a biogeographical barrier. 101 102 Results and discussion 103 104 Overview of taxonomic biogeography 105 106 6.6 Gbp of 454 sequence data representing microorganisms in the size range 0.1 – 3.0 µm was 107 obtained from 16 samples. After removal of low-quality reads, 454 sequencing yielded 157,507 108 to 597,689 reads per sample (mean 354,399) of lengths ranging from 100 to 606 bp (mean 378). 109 The proportion of reads in each sample which yielded matches to RefSeq ranged from 25% to 110 85% (mean 62%). The most abundant OTUs in each sample are given in Table 1 and a full list of 111 OTU abundances in Table S2. It is important to note that the taxonomic assignments are 112 confident assignments ( i.e. below an E-value threshold of 1.0 × 10 -3) that are limited to the 113 sequences of organisms available in the database and identified by MINSPEC as part of the 114 minimal species set. 5 Wiley-Blackwell and Society for Applied Microbiology Page 6 of 848 115 ANOSIM was performed to test for statistically significant differences between the OTU 116 profiles of the zones.
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