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Effect of the Environment on Horizontal Gene Transfer Between Bacteria and Archaea C

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Effect of the Environment on Horizontal Gene Transfer Between Bacteria and Archaea C Effect of the Environment on Horizontal Gene Transfer between Bacteria and Archaea C. A. Fuchsman, R.E. Collins1, W.J. Brazelton2 and G. Rocap [email protected] 1. Present address: University of Alaska Fairbanks School of Oceanography, University of Washington 2. Present address: University of Utah Who Shares Unusually Large #s of Genes? What Genes are Horizontally Transferred? Where is the Transfer Happening? Abstract Difference between Bacteria over the 95% CI Functional Gene Categories Isolation environment for bacteria > 95% CI from Horizontal gene transfer, the transfer and incorporation of & the bacterial dataset genetic material between different species is important in average for horizontally transferred genes Whole Dataset Bacteria with many the evolution and adaption of microbes to their environment. shared genes 448 bacterial and 57 archaeal genomes were compared using Lifestyle reciprocal BLAST hits. By removing the effect of genome size in the bacteria, we have identified bacteria with unusually large numbers of shared genes with archaea for their genome size. Archaea and bacteria that live in anaerobic and/or high temperature conditions are more likely to share unusually large numbers of genes. The DarkHorse algorithm, a probability based lineage-weighted method (Podell and Gaasterland, 2007), identified potential horizontally transferred genes between archaea and bacteria. Archaea and bacteria that live in anaerobic and/or high temperature conditions are more likely to share horizontally transferred genes. This is mainly due Environment of Culture Isolation Horizontally tranferred genes are enriched in inorganic ion transfer to horizontal gene transfer of genes from the archaea to the and energy metabolism. Enriched: hot springs, sediment, soil bacteria. Horizontally transferred genes are enriched in the Shared genes are enriched in translation and nucleotide metabolism, functional gene categories inorganic ion and amino acid transport These two categories are likely shared due to vertical descent. 0 from marine water, freshwater or the gut. and metabolism as well as energy conversion. Potential hotspots of horizontal gene transfer between archaea and bacteria include Bacteria Who Donated the Transferred Genes? hotsprings, sediments, and oil wells. Cold spots for horizontal Hyperthermo Effect of Environment on Gene Transfer Aerobic Meso transfer included dilute aerobic mesophilic environments: marine Bacteria: Sediments Marine Anaerobic Meso Transfer from archaea to bacteria drives high shared gene #s Soil Salt Sludge Hot Spring Facultative Meso Food/Gut Oil Well Freshwater Hydrothermal and freshwater water column. 80 >95% CI Aerobic Thermo The DarkHorse algorithm indicates the direction of transfer. >95% CI Anaerobic Thermo Hot springs archaea Sediment archaea Facultative Thermo Bacteria and Archaea Share Genes Example: Desulfurococcus kamchatkensis 60 hyperthermophilic anaerobic HOTSPRINGS archaea Examine genes between 1 archaea and 1 bacteria 80 80 Bacteria 40 at a time Bacteria with unusually large numbers of shared genes Normal >95% CI Over 95% CI w/this archaea ( >95% CI) are preferentially ANAEROBIC THERMOPHILES Over 95% CI w/other archaea or ANAEROBIC MESOPHILES. 60 60 20 Bacteria Archaea They are also enriched in hotsprings, sediments and oil wells. Genes Transferred Horizontally Total 0 40 40 -150 -100 -50 0 50 -150 -100 -50 0 50 Shared Genes (genome size corrected) Lifestyles of archaea that share unusually large #s of 20 20 genes with bacteria Hotsprings microbes preferentially transfer genes with Archaea other hotsprings microbes. Sediment microbes preferentially transfer genes with other -10 0 0 Use BLAST (<e ) to determine similarity Genes Tranferred Horizontally Total sediment microbes. -200 -100 0 100 0 10 20 30 40 Counting these Reciprocal Best Hits avoids database bias Shared Genes (Genome Size Corrected) HGT from archaea to bacteria Repeat for 57 archaea and 450 bacteria Horizontally transferred genes correlate with shared genes. Transfer in the Marine Environment The bacteria with the most transferred genes with this anaerobic thermophilic Removing the effect of bacterial genome size archaea were also anaerobic and thermophilic. A 4 parameter log-logistic function & Example: Methanosarcina acetivorans Gradient Very little transfer 95% CI were fit for each archaeon 108 cells/g with R. Residuals were calculated. Anaerobic mesophilic MARINE SEDIMENT archaea oxic Marine 80 hot upper 95% CI 80 >95% CI anoxic cold Water column 5 line 10 106 cells/g lower 95% CI cells/g Very Little 60 60 Horizontal Gene Transfer Anaerobic Hyperthermophilic archaea 5 Lots of transfer cell counts = 10 cells/ml 40 40 Anaerobic bacteria share genes with anaerobic archaea. Thermophilic bacteria share genes with thermophilic archaea. Hydrothermal 9 Anoxic Sediment cell counts =10 cells/ml Anaerobic Mesophile Bacteria and archaea with similar lifestyles share genes. 20 20 Vent Supported by two-way ANOSIM p=0.001. Lots of Horizontal Gene Transfer High cell abundances increases transfer rates in biofilms. Total Horizontally Tranferred Genes Tranferred Horizontally Total 0 0 Attached microbes secrete polysaccharides that localize free DNA -200 -100 0 100 0 20 40 60 80 Which archaea share the most or least genes with bacteria? (Molin and Tolker-Nielsen, 2003; Aminov, 2011) Shared Genes (Genome Size Corrected) HGT from archaea to bacteria High Salt (aerobic) Lifestyle Archaea Isolation Archaea There is high virus production and abundance in sediments Anaerobic Thermophile Marine Hot Springs Horizontal transfer from archaea dominates in bacteria with large # of shared genes (Danovaro et al., 2008) Anaerobic Mesophile High Salt Hydrothermal 30 Aerobic Thermophile Freshwater Sediment The bacteria with the most transferred genes with this anaerobic mesophilic ∴Not surprisingly horizontal gene transfer between archaea and Aerobic Mesophile Other Soil I Gut archaea were also anaerobic and mesophilic bacteria is lower in the aerobic dilute environments like the A small genome is an adaptive strategy that allows a C 25 marine water column. microbe to use fewer nutrients & replicate faster. Microbes % 5 Transfer by both domains-- Example: Aeropyrum pernix 9 with small genomes expel unused genes (Giovannoni et al., e h t 20 Aerobic hyperthermophilic HYDROTHERMAL VENT archaea 2005). r 80 Aerobic e v Thermophiles Conclusions: A large genome is an adaptive strategy that allows more o Increasing a 15 i • Anaerobic and thermophilic bacteria share unusually versatility. Microbes with large genomes may keep excess r Oxygen e t 60 genes (Chang et al., 2011). c large numbers of genes with archaea. a 10 High Salt B # To include a range of adaptations, we remove the 40 Marine watercolumn • Gene transfer from archaea to bacteria that live in affect of genome size. 5 10 20 30 40 50 10 20 30 40 50 similar oxygen concentration and temperature Average # shared genes over the 95% CI Average # shared genes over the 95% CI 20 conditions may explain these large #s of shared genes. Many Bacteria over the 95% CI are at the base of the Anaerobic archaea share unusual #s of genes with the most bacteria. Total Horizontally Tranferred Genes Tranferred Horizontally Total 0 phylogenetic tree Aerobic Mesophilic archaea share unusual #s of genes with the fewest bacteria. -200 -100 0 100 0 10 20 30 400 20 40 60 80 •Horizontally transferred genes between archaea and These include high salt and marine archaea. Shared Genes (Genome Size Corrected) HGT from archaea to bacteria HGT from bacteria to archaea bacteria are enriched in the categories inorganic ion Here many of the bacteria with unusual #s of shared genes had transferred genes transfer and energy metabolism. from archaea to bacteria BUT some were transferred from the bacteria to archaea Note: the bacteria transferring genes TO archaea were aerobic thermophiles Where do the Shared Genes Come From? • Potential hotspots of horizontal gene transfer between Example: Nitrosopumilus maritimus 80 archaea and bacteria include hotsprings, sediments, 1) Vertical Descent-- a common ancestor had this gene Aerobic mesophilic and oil wells. Of course some genes are shared due to vertical descent: >95% CI MARINE archaea Mantel test indicates similarily between shared genes & 16S rDNA 60 distances but the R value is small (R=0.176 p=0.0000) • Cold spots for horizontal transfer included dilute 40 aerobic mesophilic environments: marine and 2) Horizontal Gene Transfer-- genes transferred between domains of life freshwater water column. a) Bacteria or archaea can pick up free DNA from the environment b) Viruses can transfer DNA between domains of life 20 Bacteria over the 95% CI (Prangishvili et al., 2006) with Nitrosopumilus were References not aerobic mesophiles. Aminov (2011) Frontiers in Microbiology 2: 158. Horizontally transferred genes were identified using DarkHorse, a statistical 0 Chang et al. (2011) Stand. Genomic Sci. 5: 97–111 Total Horizontally Tranferred Genes Tranferred Horizontally Total Danovaro et al. (2008) Nature 454: 1084-1088. method which calculates phylogenetic distance between the query and its closest -200 -100 0 1000 10 20 30 Giovannoni et al. (2005) Science 309: 1242–5. database match (Podell &Gaasterland, 2007). Shared Genes (Genome Size Corrected) HGT from archaea to bacteria Molin &Tolker-Nielsen (2003) Curr. Opin. Biotechnol. 14: 255–261 Bacterial Dataset Podell &Gaasterland (2007) Genome Biol. 8: R16 In general, transfer from archaea drive unusually large #s of shared genes in bacteria Prangishvili et al. (2006) Nat. Rev. Microbiol. 4: 837–848 Thanks to Michael Carlson..
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