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Effect of the Environment on Horizontal Gene Transfer between Bacteria and ArchaeaC. A. Fuchsman, R.E. Collins1, W.J. Brazelton2 and G. Rocap [email protected]
School of Oceanography, University of Washington
Abstract Horizontal gene transfer, the transfer and incorporation of genetic material between different species is important in the evolution and adaption of microbes to their environment. 448 bacterial and 57 archaeal genomes were compared using reciprocal BLAST hits. By removing the effect of genome size in the bacteria, we have identified bacteria with unusuallylarge 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 to horizontal gene transfer of genes from the archaea to the bacteria. Horizontally transferred genes are enriched in the functional gene categories inorganic ion and amino acid transport and metabolism as well as energy conversion. Potential hotspots of horizontal gene transfer between archaea and bacteria include hotsprings, sediments, and oil wells. Cold spots for horizontal transfer included dilute aerobic mesophilic environments: marine and freshwater water column.
Conclusions: • Anaerobic and thermophilic bacteria share unusually large numbers of genes with archaea. • Gene transfer from archaea to bacteria that live insimilar oxygen concentration and temperature conditions may explain these large #s of shared genes.
•Horizontally transferred genes between archaea and bacteria are enriched in the categories inorganic ion transfer and energy metabolism.
• Potential hotspots of horizontal gene transfer between archaea and bacteria include hotsprings, sediments, and oil wells.
• Cold spots for horizontal transfer included dilute aerobic mesophilic environments: marine and freshwater water column.
1. Present address: University of Alaska Fairbanks 2. Present address: University of Utah
Bacteria and Archaea Share Genes
What Genes are Horizontally Transferred?Functional Gene Categories
Horizontally tranferred genes are enriched in inorganic ion transferand energy metabolism. Shared genes are enriched in translation and nucleotide metabolism,These two categories are likely shared due to vertical descent.
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SedimentsSoilFood/Gut
SludgeFreshwater
MarineSaltOil Well
Hot SpringHydrothermal
Hot springs archaea Sediment archaea
Effect of Environment on Gene Transfer
Shared Genes (genome size corrected)
Hotsprings microbes preferentially transfer genes with other hotsprings microbes.Sediment microbes preferentially transfer genes with othersediment microbes.
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Bacteria:
Anaerobic bacteria share genes with anaerobic archaea.Thermophilic bacteria share genes with thermophilic archaea.
Lifestyles of archaea that share unusually large #s ofgenes with bacteria
Archaea
Bacteria and archaea with similar lifestyles share genes.Supported by two-way ANOSIM p=0.001.
Removing the effect of bacterial genome sizeA 4 parameter log-logistic function &95% CI were fit for each archaeon with R. Residuals were calculated.
A small genome is an adaptive strategy that allows a microbe to use fewer nutrients & replicate faster. Microbes with small genomes expel unused genes (Giovannoni et al., 2005). A large genome is an adaptive strategy that allows more versatility. Microbes with large genomes may keep excess genes (Chang et al., 2011).
lineupper 95% CI
lower 95% CI
High Salt (aerobic)
Anaerobic Mesophile
Anaerobic Hyperthermophilic archaea
Where do the Shared Genes Come From?1) Vertical Descent-- a common ancestor had this gene
2) Horizontal Gene Transfer-- genes transferred between domains of life a) Bacteria or archaea can pick up free DNA from the environment b) Viruses can transfer DNA between domains of life (Prangishvili et al., 2006)
Of course some genes are shared due to vertical descent: Mantel test indicates similarily between shared genes & 16S rDNA distances but the R value is small (R=0.176 p=0.0000)
Horizontally transferred genes were identified using DarkHorse, a statistical method which calculates phylogenetic distance between the query and its closest database match (Podell &Gaasterland, 2007).
>95% CI
Archaea Bacteria
Examine genes between 1 archaea and 1 bacteriaat a time
Counting these Reciprocal Best Hits avoids database bias Repeat for 57 archaea and 450 bacteria
Use BLAST (<e-10) to determine similarity
To include a range of adaptations, we remove theaffect of genome size.
Many Bacteria over the 95% CI are at the base of the phylogenetic tree
Bacterial Dataset
Gradient
anoxichot oxic
cold
Anoxic Sediment
MarineWater column
Lots of Horizontal Gene Transfer
Very Little Horizontal Gene Transfer
Lots of transfer
Very little transfer
HydrothermalVent
Transfer in the Marine Environment
cell counts =
cell counts = 105 cells/ml
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105
109 cells/ml
cells/g
cells/g cells/g
Isolation environment for bacteria > 95% CI from average for horizontally transferred genes
0 from marine water, freshwater or the gut.
Where is the Transfer Happening?
Enriched: hot springs, sediment, soil
Attached microbes secrete polysaccharides that localize free DNA(Molin and Tolker-Nielsen, 2003; Aminov, 2011)
>95% CI
∴Not surprisingly horizontal gene transfer between archaea and bacteria is lower in the aerobic dilute environments like the marine water column.
High cell abundances increases transfer rates in biofilms.
Difference between Bacteria over the 95% CI & the bacterial dataset
They are also enriched in hotsprings, sediments and oil wells.
Who Donated the Transferred Genes?
The bacteria with the most transferred genes with this anaerobic thermophilic archaea were also anaerobic and thermophilic.
Example: Desulfurococcus kamchatkensis hyperthermophilic anaerobic HOTSPRINGS archaea
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HyperthermoAerobic MesoAnaerobic MesoFacultative MesoAerobic ThermoAnaerobic ThermoFacultative Thermo
Shared Genes (Genome Size Corrected)0 10 20 30 40HGT from archaea to bacteria
NormalOver 95% CI w/this archaeaOver 95% CI w/other archaea
Bacteria
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Bacteria
>95% CI
Transfer from archaea to bacteria drives high shared gene #s
The bacteria with the most transferred genes with this anaerobic mesophilic archaea were also anaerobic and mesophilic
Horizontal transfer from archaea dominates in bacteria with large # of shared genes
Note: the bacteria transferring genes TO archaea were aerobic thermophiles
Here many of the bacteria with unusual #s of shared genes had transferred genes from archaea to bacteria BUT some were transferred from the bacteria to archaea
Horizontally transferred genes correlate with shared genes.
Example: Methanosarcina acetivoransAnaerobic mesophilic MARINE SEDIMENT archaea
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Shared Genes (Genome Size Corrected)
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Transfer by both domains-- Example: Aeropyrum pernixAerobic hyperthermophilic HYDROTHERMAL VENT archaea
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Shared Genes (Genome Size Corrected)-200 -100 0 100
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0 10 20 30 40HGT from archaea to bacteria
0 20 40 60 80HGT from bacteria to archaea
AerobicThermophiles
Example: Nitrosopumilus maritimus
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0 10 20 30HGT from archaea to bacteria
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Shared Genes (Genome Size Corrected)
>95% CI
Bacteria over the 95% CIwith Nitrosopumilus were not aerobic mesophiles.
Aerobic mesophilic MARINE archaea
In general, transfer from archaea drive unusually large #s of shared genes in bacteria
Environment of Culture Isolation
Lifestyle
Whole Dataset Bacteria with many shared genes
Bacteria with unusually large numbers of shared genes ( >95% CI) are preferentially ANAEROBIC THERMOPHILES or ANAEROBIC MESOPHILES.
There is high virus production and abundance in sediments (Danovaro et al., 2008)
Who Shares Unusually Large #s of Genes?
ReferencesAminov (2011) Frontiers in Microbiology 2: 158.Chang et al. (2011) Stand. Genomic Sci. 5: 97–111Danovaro et al. (2008) Nature 454: 1084-1088.Giovannoni et al. (2005) Science 309: 1242–5.Molin &Tolker-Nielsen (2003) Curr. Opin. Biotechnol. 14: 255–261Podell &Gaasterland (2007) Genome Biol. 8: R16Prangishvili et al. (2006) Nat. Rev. Microbiol. 4: 837–848 Thanks to Michael Carlson.
The DarkHorse algorithm indicates the direction of transfer.
Aerobic Mesophilic archaea share unusual #s of genes with the fewest bacteria. These include high salt and marine archaea.
Anaerobic archaea share unusual #s of genes with the most bacteria.
10 20 30 40 50Average # shared genes over the 95% CI
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Anaerobic ThermophileAnaerobic MesophileAerobic ThermophileAerobic Mesophile
10 20 30 40 50Average # shared genes over the 95% CI
Hot SpringsHydrothermalSedimentSoilGut
MarineHigh SaltFreshwaterOther
IncreasingOxygen
Archaea Archaea
High Salt
Marine watercolumn
Which archaea share the most or least genes with bacteria?IsolationLifestyle
