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Increased rates of horizontal gene transfer in psychrophile genomes and potential links to the Phanerozoic climate record Jeff S. Bowman, Eric Collins, Jody W. Deming [email protected] Why HGT might be elevated in psychrophile genomes Introduce method for evaluating genomic plasticity in a population Application of this method, psychrophiles vs. mesophiles Potential links between gene acquisition and the Phanerozoic climate record

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Increased rates of horizontal gene transfer in psychrophilic genomes and potential links to the Phanerozoic climate record Bowman, JS, Collins, RE, Deming, JW Several authors have suggested that the rate of horizontal gene transfer (HGT) may be elevated in cold adapted Bacteria and Archaea, a hypothesis supported by a growing number of genome-genome comparisons between related psychrophilic and mesophilic strains. An increased rate of HGT may be the result of widespread lysogeny and pseudolysogeny among high latitude phage, selective pressure imposed by increased environmental stress, the sympagic nature of cold microbial habitats such as sea ice, or a combination of these factors. To more broadly test this hypothesis, and establish a method for further analysis, we developed a new approach to quantify the degree of genome plasticity in microbial populations, based on the divergence of predicted proteomes compared to the divergence of 16S rRNA genes. Applying this method to a group of 20 psychrophilic genomes and a taxonomically related mesophilic control group we found genome plasticity to be significantly higher in the cold group (p = 3.5 x 10-6). To place these findings in an evolutionary context we used the GC amelioration technique to date the acquisition of coding sequences (CDS) with anomalous GC content in both the psychrophile and control groups. For the control group the dates of acquisition of anomalous CDS were not correlated with cold periods during the last 650 million years (p = 0.234) while anomalous CDS in the psychrophilic group had a robust relationship (p = 0.006). Many of the CDS in this group that were predicted to have undergone HGT during cold periods code for transposases, suggesting a link between historic HGT events and current patterns of HGT among cold adapted microbial populations.

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Increased rates of horizontal gene transfer in psychrophile genomes and potential links to the Phanerozoic climate record

Jeff S. Bowman, Eric Collins, Jody W. Deming

[email protected]

• Why HGT might be elevated in psychrophile genomes • Introduce method for evaluating genomic plasticity in a

population • Application of this method, psychrophiles vs. mesophiles • Potential links between gene acquisition and the

Phanerozoic climate record

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Why HGT might be elevated in cold environments

Junge et al. 2001

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-15 °C

Wells and Deming, 2006

HGT may be elevated by phage-bacteria and bacteria-bacteria contact rates in ice environments

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HGT may be elevated by phage-bacteria and bacteria-bacteria contact rates in ice environments

Infection rates and phage diversity may be higher in low temperature environments

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Anesio and Bellas, 2011

Why HGT might be elevated in cold environments

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Method for evaluating genomic plasticity in a population

Quantifying genomic plasticity

Are psychrophiles more genetically plastic than mesophiles?

Bowman et al., 2014, in prep 4

Genomic plasticity = gene loss + HGT + gene duplication

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Method for evaluating genomic plasticity in a population

Maximum-likelihood tree of psychrophile and mesophile strains used in this analysis Bowman et al., 2014, in prep

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Method for evaluating genomic plasticity in a population

Bowman et al., 2014, in prep

divG = abs(16S – CV) 16S: 16S distance CV: amino acid compositional vector distance (Qi et al., 2004) Values transformed • mean = 0 • variance = 1 • range between 0

and 1

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Method for evaluating genomic plasticity in a population

Bowman et al., 2014, in prep

divG = abs(16S – CV) 16S: 16S distance CV: amino acid compositional vector distance (Qi et al., 2004) Values transformed • mean = 0 • variance = 1 • range between 0

and 1

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Transposase (blue)

Integrase/ Recombinase (green)

Phage specific

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Chapter 5 – Horizontal gene transfer (HGT) in psychrophile genomes

Bowman et al., 2014, in prep

divG = abs(16S – CV) 16S: 16S distance CV: amino acid compositional vector distance (Qi et al., 2004) Values transformed • mean = 0 • variance = 1 • range between 0

and 1

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Octadecabacter antarcticus divG = 0.09

Octadecabacter arcticus

divG = 0.25

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Results, psychrophiles vs. mesophiles

Blue = psychrophiles, Orange = mesophiles • Distribution of 16S distances nearly identical between the two groups • Distribution of compositional vectors distances, divG, and divG are all

significantly different (p = 2.49 x 10-8, 3.5 x 10-6, 0.01) by the Mann-Whitney or Students T-tests

• Preliminary (limited sample size) evidence for enhanced plasticity in psychrophile genomes

Bowman et al., 2014, in prep 9

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Estimating time since acquisition for probable HGT events

During glacial maximum… • Psychrophile range is expanded • More ice environments • More temperate phage?

Veizer et al., 2003

Temperature anomalies during Phanerozoic Eon

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Estimating time since acquisition for probable HGT events

Bowman et al., 2014, in prep

Distribution of HGT event probabilities

• Identify likely HGT events by anomalous GC content

• Estimate time since acquisition with GC amelioration method (Lawrence and Ochman, 1997)

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GC

anom

aly

Psychrophiles

Mesophiles

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Estimating time since acquisition for probable HGT events

= period when Earth’s temp was below the current mean

= mass extinction event

= 10 My running mean

Psychrophiles

Mesophiles

Monte-Carlo analysis for psychrophiles

562.74

-757.61

Bowman et al., 2014, in prep 12

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Conclusions + acknowledgements

• Developed a new method for evaluating genomic plasticity between populations

• Preliminary evidence for higher genomic plasticity among psychrophiles compared to mesophiles

• For psychrophiles, strong correlation between time since acquisition for putative HT genes and geologic cold periods

This presentation and code for methods linked from: www.ldeo.columbia.edu/~bowmanjs