Download Effect of the Environment on Horizontal Gene Transfer

Effect of the Environment on Horizontal Gene Transfer between Bacteria and Archaea
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[email protected]
C. A. Fuchsman, R.E. Collins , W.J. Brazelton and G. Rocap
1. Present address: University of Alaska Fairbanks
2. Present address: University of Utah
School of Oceanography, University of Washington
What Genes are Horizontally Transferred?
Who Shares Unusually Large #s of Genes?
Difference between Bacteria over the 95% CI
& the bacterial dataset
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 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
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.
Lifestyle
Horizontally tranferred genes are enriched in inorganic ion transfer
and energy metabolism.
Shared genes are enriched in translation and nucleotide metabolism,
These two categories are likely shared due to vertical descent.
Environment of Culture Isolation
Bacteria
Hyperthermo
Aerobic Meso
Anaerobic Meso
Facultative Meso
Aerobic Thermo
Anaerobic Thermo
Facultative Thermo
Bacteria with unusually large numbers of shared genes
( >95% CI) are preferentially ANAEROBIC THERMOPHILES
or ANAEROBIC MESOPHILES.
Bacteria
They are also enriched in hotsprings, sediments and oil wells.
Lifestyles of archaea that share unusually large #s of
genes with bacteria
Archaea
Use BLAST (<e-10) to determine similarity
Counting these Reciprocal Best Hits avoids database bias
Repeat for 57 archaea and 450 bacteria
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Total Horizontally Tranferred Genes
Examine genes between 1 archaea and 1 bacteria
at a time
lower 95% CI
Anaerobic Hyperthermophilic archaea
Anaerobic bacteria share genes with anaerobic archaea.
Thermophilic bacteria share genes with thermophilic archaea.
Bacteria and archaea with similar lifestyles share genes.
Supported by two-way ANOSIM p=0.001.
Anaerobic Mesophile
Which archaea share the most or least genes with bacteria?
Anaerobic Thermophile
Anaerobic Mesophile
Aerobic Thermophile
Aerobic Mesophile
Isolation
Archaea
Marine
High Salt
Freshwater
Other
Hot Springs
Hydrothermal
Sediment
Soil
Gut
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15
Increasing
Oxygen
High Salt
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Marine watercolumn
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10
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50 10
20
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Average # shared genes over the 95% CI Average # shared genes over the 95% CI
Anaerobic archaea share unusual #s of genes with the most bacteria.
Aerobic Mesophilic archaea share unusual #s of genes with the fewest bacteria.
These include high salt and marine archaea.
Where do the Shared Genes Come From?
1) Vertical Descent-- a common ancestor had this gene
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)
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)
Bacterial Dataset
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20
20
Bacteria
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).
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80
>95% CI
Sediment archaea
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20
0
-150
-100
-50
0
50
-150
-100
-50
Shared Genes (genome size corrected)
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50
Hotsprings microbes preferentially transfer genes with
other hotsprings microbes.
Sediment microbes preferentially transfer genes with other
sediment microbes.
Transfer in the Marine Environment
Gradient
108
cells/g
hot
anoxic
105
cells/g
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60
Lots of transfer
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Hot Spring
Hydrothermal
Sludge
Freshwater
>95% CI
Hot springs archaea
Example: Methanosarcina acetivorans
Anaerobic mesophilic MARINE SEDIMENT archaea
>95% CI
Marine
Salt
Oil Well
Sediments
Soil
Food/Gut
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Normal
Over 95% CI w/this archaea
Over 95% CI w/other archaea
Very little transfer
Marine
Water column
oxic
cold
106
cells/g
Very Little
Horizontal Gene Transfer
cell counts = 105 cells/ml
40
Hydrothermal
Vent
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0
0
0
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40
60
80
-200
-100
0
100
HGT from archaea to bacteria
Shared Genes (Genome Size Corrected)
Horizontal transfer from archaea dominates in bacteria with large # of shared genes
The bacteria with the most transferred genes with this anaerobic mesophilic
archaea were also anaerobic and mesophilic
Transfer by both domains-- Example: Aeropyrum pernix
Aerobic hyperthermophilic HYDROTHERMAL VENT archaea
Aerobic
Thermophiles
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cell counts =109 cells/ml
Anoxic Sediment
Lots of Horizontal Gene Transfer
High cell abundances increases transfer rates in biofilms.
Attached microbes secrete polysaccharides that localize free DNA
(Molin and Tolker-Nielsen, 2003; Aminov, 2011)
There is high virus production and abundance in sediments
(Danovaro et al., 2008)
∴Not surprisingly horizontal gene transfer between archaea and
bacteria is lower in the aerobic dilute environments like the
marine water column.
Conclusions:
• Anaerobic and thermophilic bacteria share unusually
large numbers of genes with archaea.
• Gene transfer from archaea to bacteria that live in
similar oxygen concentration and temperature
conditions may explain these large #s of shared genes.
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0
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40
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80
-200
-100
0
100 0
10
20
30
40 0
HGT from bacteria to archaea
Shared Genes (Genome Size Corrected) HGT from archaea to bacteria
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
Note: the bacteria transferring genes TO archaea were aerobic thermophiles
Total Horizontally Tranferred Genes
Many Bacteria over the 95% CI are at the base of the
phylogenetic tree
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Archaea
Total Horizontally Tranferred Genes
To include a range of adaptations, we remove the
affect of genome size.
Lifestyle
# Bacteria over the 95% CI
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).
>95% CI
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40
60
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Example: Desulfurococcus kamchatkensis
hyperthermophilic anaerobic HOTSPRINGS archaea
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80
Bacteria:
The DarkHorse algorithm indicates the direction of transfer.
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0
-200
-100
0
100
0
10
20
30
40
HGT from archaea to bacteria
Shared Genes (Genome Size Corrected)
Total Horizontally Tranferred Genes
upper 95% CI
line
Effect of Environment on Gene Transfer
Transfer from archaea to bacteria drives high shared gene #s
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A 4 parameter log-logistic function &
95% CI were fit for each archaeon
with R. Residuals were calculated.
Enriched: hot springs, sediment, soil
0 from marine water, freshwater or the gut.
Who Donated the Transferred Genes?
Horizontally transferred genes correlate with shared genes.
The bacteria with the most transferred genes with this anaerobic thermophilic
archaea were also anaerobic and thermophilic.
Removing the effect of bacterial genome size
High Salt (aerobic)
Isolation environment for bacteria > 95% CI from
average for horizontally transferred genes
Bacteria with many
shared genes
Whole Dataset
Bacteria and Archaea Share Genes
Archaea
Functional Gene Categories
Total Horizontally Transferred Genes
Abstract
Where is the Transfer Happening?
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Example: Nitrosopumilus maritimus
Aerobic mesophilic
MARINE archaea
>95% CI
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20
Bacteria over the 95% CI
with Nitrosopumilus were
not aerobic mesophiles.
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-200
-100
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100 0
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Shared Genes (Genome Size Corrected) HGT from archaea to bacteria
In general, transfer from archaea drive unusually large #s of shared genes in bacteria
•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.
References
Aminov (2011) Frontiers in Microbiology 2: 158.
Chang et al. (2011) Stand. Genomic Sci. 5: 97–111
Danovaro et al. (2008) Nature 454: 1084-1088.
Giovannoni et al. (2005) Science 309: 1242–5.
Molin &Tolker-Nielsen (2003) Curr. Opin. Biotechnol. 14: 255–261
Podell &Gaasterland (2007) Genome Biol. 8: R16
Prangishvili et al. (2006) Nat. Rev. Microbiol. 4: 837–848
Thanks to Michael Carlson.