In the case of the nitrogen cycle, high-throughput oxidation of reduced substrates
such as ammonium/ammonia, aliphatic amines, as well as urea (Fig. 9.1) led to fast
accumulation of highly toxic (nitric oxide), mutagenic (hydroxylamine or “aminol”)
or explosive (hydrazine) intermediates that demanded detoxification by either reduction or oxidation reactions. Detox by further reduction of reduced intermediates
would deprive the cell of precious reducing power without exploiting these intermediates catabolically. In contrast, detox by oxidation and channeling of the
extracted electrons to a sufficient reservoir of intracellular electron acceptors
would preserve catabolic opportunities. This was successfully accomplished by the
modular coupling with QRP complexes facilitating high-throughput electron flow in
and out of the quinone pool to respiratory acceptors, thereby generating enough
proton-motive force needed to support reverse electron flow to fuel carbon and
nitrogen assimilation. The fixation of carbon and nitrogen into biomass are the two
costliest anabolic tasks cells have to master, and they can afford catabolism with
narrow differences between their oxidation and terminal reduction potentials only
when they exist in highly reduced environments and have access to methane (CH 4 )
and ammonium (NH 4
+
). In our present predominantly oxic world, oxygen is available and well suited to serve as co-substrate and terminal acceptor at high-throughput
energy- and electron-harvesting and electron-disposing ends, respectively, of the
catabolic pipeline, which generates greater differences between catabolic oxidation
and terminal reduction potentials. Broader implementation of this opportunity
required the emergence of a great diversity of QRP complexes suited to match
particular donor and acceptor environments, and this diversity could not have arisen
at once during the Great Oxygenation Event (GOE) about 2.5 billion years ago.
Therefore, the individual modular components of the pipeline must have evolved
and been functional during anoxic times before the GOE, and some likely evolved
separately in different genomic backgrounds. Subsequently, horizontal gene transfers then occurred at the “right time,” the “right place,” and the “right frequency” to
fit cassettes poised at the proper redox potential into an expanded new module to
provide the recipient cell with an advantage for succession in its present or emerging
new environment.
Enzyme complexes generally operate bidirectionally, driven by the redox and
energy gradients in which they operate. This is why individual cassettes could be
“fitted” into different catabolic contexts as long as the intersections met with correct
redox potentials, thereby creating diverse linear and branched modules with varying
entering and exiting redox potentials that were accomplished, in part, by the emergence of a diverse complement perfectly suited for metabolic innovation. This
modular design permitted metabolic collaboration between functional cassettes
within cells, between different cells in a population and between populations of
different cells, which provided for closed cycles as well as for segments of cycles.
The extant nitrogen cycle more likely than not existed unclosed during the vast
anoxic period before the GOE when copper was not largely bioavailable and the only
known enzyme capable of reducing nitrous oxide (laughing gas) to dinitrogen, the
copper enzyme complex nitrous oxide reductase, was not yet invented or operational. This missing connection between the inert reservoir of dinitrogen and the
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M. G. Klotz and L. Y. Stein
such as ammonium/ammonia, aliphatic amines, as well as urea (Fig. 9.1) led to fast
accumulation of highly toxic (nitric oxide), mutagenic (hydroxylamine or “aminol”)
or explosive (hydrazine) intermediates that demanded detoxification by either reduction or oxidation reactions. Detox by further reduction of reduced intermediates
would deprive the cell of precious reducing power without exploiting these intermediates catabolically. In contrast, detox by oxidation and channeling of the
extracted electrons to a sufficient reservoir of intracellular electron acceptors
would preserve catabolic opportunities. This was successfully accomplished by the
modular coupling with QRP complexes facilitating high-throughput electron flow in
and out of the quinone pool to respiratory acceptors, thereby generating enough
proton-motive force needed to support reverse electron flow to fuel carbon and
nitrogen assimilation. The fixation of carbon and nitrogen into biomass are the two
costliest anabolic tasks cells have to master, and they can afford catabolism with
narrow differences between their oxidation and terminal reduction potentials only
when they exist in highly reduced environments and have access to methane (CH 4 )
and ammonium (NH 4
+
). In our present predominantly oxic world, oxygen is available and well suited to serve as co-substrate and terminal acceptor at high-throughput
energy- and electron-harvesting and electron-disposing ends, respectively, of the
catabolic pipeline, which generates greater differences between catabolic oxidation
and terminal reduction potentials. Broader implementation of this opportunity
required the emergence of a great diversity of QRP complexes suited to match
particular donor and acceptor environments, and this diversity could not have arisen
at once during the Great Oxygenation Event (GOE) about 2.5 billion years ago.
Therefore, the individual modular components of the pipeline must have evolved
and been functional during anoxic times before the GOE, and some likely evolved
separately in different genomic backgrounds. Subsequently, horizontal gene transfers then occurred at the “right time,” the “right place,” and the “right frequency” to
fit cassettes poised at the proper redox potential into an expanded new module to
provide the recipient cell with an advantage for succession in its present or emerging
new environment.
Enzyme complexes generally operate bidirectionally, driven by the redox and
energy gradients in which they operate. This is why individual cassettes could be
“fitted” into different catabolic contexts as long as the intersections met with correct
redox potentials, thereby creating diverse linear and branched modules with varying
entering and exiting redox potentials that were accomplished, in part, by the emergence of a diverse complement perfectly suited for metabolic innovation. This
modular design permitted metabolic collaboration between functional cassettes
within cells, between different cells in a population and between populations of
different cells, which provided for closed cycles as well as for segments of cycles.
The extant nitrogen cycle more likely than not existed unclosed during the vast
anoxic period before the GOE when copper was not largely bioavailable and the only
known enzyme capable of reducing nitrous oxide (laughing gas) to dinitrogen, the
copper enzyme complex nitrous oxide reductase, was not yet invented or operational. This missing connection between the inert reservoir of dinitrogen and the
154
M. G. Klotz and L. Y. Stein