Understanding bacterial adaptation to aerobic and anaerobic environments through experimental evolution and whole genome analysis : a thesis presented in fulfilment of the requirements for the degree of Doctor of Philosophy in Genetics at Massey University, Palmerston North, New Zealand
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Date
2014
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Massey University
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Abstract
Facultative anaerobic organisms have the metabolic versatility to grow in both aerobic and
anaerobic environments. However, molecular mechanisms that underpin adaptation to anaerobic
environments are not well understood. This study aims to understand how the facultative
anaerobe, Escherichia coli, adapts to environments that vary in oxygen content. An experimental
evolution experiment was conducted in which replicate lineages were established from a preevolved
clonal culture of E. coli REL4536. Lineages were serially sub-cultured for 4,000 generations
within strict aerobic and strict anaerobic environments, and a treatment that fluctuated between
the two environments. Significant increases in the relative fitness of lineages exposed to anaerobic
conditions were observed, whereas the relative fitness of lineages in aerobic conditions did not
increase, likely as the ancestor had been pre-adapted to aerobic growth.
Mutations that arose during evolution were identified by genome sequencing randomly-selected
clones from each lineage at 2,000 and 4,000 generations. Traits that contributed to adaptation
were predicted via the occurrence of independent mutations affecting common traits among
lineages. Adaptation to the anaerobic environment was facilitated by modifications to anaerobic
fermentation and the inactivation of virulence genes, whereas in the aerobic environment,
mutations predicted to confer a growth advantage in stationary phase were observed. The
evolution of generalists involved traits that were similar to those found in both aerobic and
anaerobically evolved lineages, as well as the deletion of cryptic prophages from the genome and
modifications to amino acid transport.
Phenotypically distinct small colony morphotypes (SCM) arose within anaerobic lineages and two
separate adaptive pathways are hypothesised for this divergence. SCM1 were capable of stable coexistence
with co-evolved cells of typical colony morphotype, most likely through an acetate crossfeeding
mechanism. In contrast, SCM2 was able to out-compete the ancestor within 14 days,
despite exhibiting a lower growth rate than the ancestor. SCM2 likely evolved the ability to inhibit
the ancestral strain through a contact dependent inhibition mechanism, as evidenced by a
mutation in glgC. This thesis demonstrates the complex nature of adaptation to anaerobic
environments, as revealed by experimental evolution and whole genome sequencing.
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Keywords
Escherichia coli, Anaerobic bacteria, Genetics, Evolution, Adaptation, Research Subject Categories::NATURAL SCIENCES::Biology::Cell and molecular biology::Genetics