People often think of evolution as increasing complexity, but from the microbial point of view, simplicity is a fitness advantage. “The photosynthesizing cyanobacteria [in genus] Prochlorococcus, for example, are some of the genetically wimpiest bacteria in the world. Left to their own devices, these little cells would have an exceedingly difficult time just staying alive, and yet they're the most abundant photosynthesizing organisms on Earth,” says J. Jeffrey Morris, from Richard Lenski's lab at Michigan State University in East Lansing.
Morris and his colleagues initially watched thousands of generations of replicating Escherichia coli, a stand in for ocean-dwelling Prochlorococcus, cope with hydrogen peroxide and showed that helper cells leaking the hydrogen peroxide–detoxifying enzyme KatG enabled beneficiary bacteria to reduce their genomes and, therefore, to replicate with greater efficiency. They call this “the black queen hypothesis” (BQH), after the queen of spades in the game of hearts—the costly card everyone wants to avoid.
In contrast to the arms race described by the red queen hypothesis (doi:10.1093/biosci/biu066), the BQH is a passive affair. “Species are in a ‘race to the bottom,’ deleting the genes for as many costly functions as they can get away with,” Morris explains.
In their latest study (doi:10.1111/evo.12485), these researchers tested and confirmed the central prediction of the BQH: Normally competing bacterial strains can stably coexist because of the shared public goods produced by leaky producer cells—in this case, KatG—which these researchers describe as a form of cooperation.
“This is important because there isn't any long-term structure in open ocean microbial communities, and traditional evolutionary theory predicts that you wouldn't see any cooperation. But in reality,” claims Morris, “there's tons of cooperation around.”
For example, many microbial plankton species have jettisoned the genes needed to produce one or more essential vitamins and instead outsource them from or exchange them with other cells in their environment, says Stephen J. Giovannoni, from Oregon State University, in Corvallis. He argues that “most of the time, the fitness advantages of smaller genomes and lower cell replicating costs offset the potential fitness gains that would come from vitamin manufacture when the required nutrients are in short supply.”
As is exemplified by Prochlorococcus, extensive gene loss exists even among Cyanobacteria, a group that otherwise contains some of the most complex bacteria on Earth. But the reconstruction of archaeal genomes provides the most compelling evidence for the dominance of genome reduction and simplification in nature, according to Eugene V. Koonin and Yuri Wolf, at the National Institutes of Health's National Center for Biotechnology Information. “The pattern of gene loss and gain in archaea is not trivial; there seems to have been some net gain at the base of each major archaeal branch that was invariably followed by substantial gene loss,” they note in the journal Bioessays (doi:10.1002/bies.201300037).
Furthermore, when ancient Cyanobacteria were domesticated by the ancestors of plants, the bacteria deleted most of their genes or transferred them to the host nucleus, becoming chloroplasts, and, along with mitochondria, are considered “the ultimate realization of bacterial reductive evolution,” Koonin says. The association “dramatically increased the habitat of these photosynthetic bacteria from the sea to terrestrial ecosystems” and enabled plants to colonize the Earth, according to Ton Bisseling, at King Saud University, in Riyadh, Saudi Arabia, writing in Science (doi:10.1126/science.1256542).
Notably, though, in contrast to most other forms of microbial cooperation, BQH participants make no commitments. “At first glance, you might think that the interaction we studied involves altruism or, perhaps, some sort of reciprocal benefits. However, we know the initial state of the system, and we saw how it evolved over time in the lab. So we know the coexistence of the two [competing] bacterial types depends on the detoxification—on the protection—provided by the black queen function. Because that function is leaky, the detoxifiers can't help but produce a public good, and the beneficiaries simply take advantage of the cleaned-up environment to lose costly genes,” according to Lenski.
Giovannoni comments on the importance of “streamlining theory” to the BQH, explaining that it originally showed how gene loss works. He also notes that, although “some lost functions make interactions more complicated in ways predicted by the BQH, others enable cells to use resources more efficiently, without increasing interaction.”
“The concept of streamlining had little traction before the discovery of small-genome microbial cells in the oceans caused a shift in perceptions, putting greater emphasis on the high cost of metabolic functions in some ecosystems,” he says.
People often think of evolution as increasing complexity, but from the microbial point of view, simplicity is a fitness advantage. “The photosynthesizing cyanobacteria [in genus] Prochlorococcus, for example, are some of the genetically wimpiest bacteria in the world. Left to their own devices, these little cells would have an exceedingly difficult time just staying alive, and yet they're the most abundant photosynthesizing organisms on Earth,” says J. Jeffrey Morris, from Richard Lenski's lab at Michigan State University in East Lansing.
Morris and his colleagues initially watched thousands of generations of replicating Escherichia coli, a stand in for ocean-dwelling Prochlorococcus, cope with hydrogen peroxide and showed that helper cells leaking the hydrogen peroxide–detoxifying enzyme KatG enabled beneficiary bacteria to reduce their genomes and, therefore, to replicate with greater efficiency. They call this “the black queen hypothesis” (BQH), after the queen of spades in the game of hearts—the costly card everyone wants to avoid.
In contrast to the arms race described by the red queen hypothesis (doi:10.1093/biosci/biu066), the BQH is a passive affair. “Species are in a ‘race to the bottom,’ deleting the genes for as many costly functions as they can get away with,” Morris explains.
In their latest study (doi:10.1111/evo.12485), these researchers tested and confirmed the central prediction of the BQH: Normally competing bacterial strains can stably coexist because of the shared public goods produced by leaky producer cells—in this case, KatG—which these researchers describe as a form of cooperation.
“This is important because there isn't any long-term structure in open ocean microbial communities, and traditional evolutionary theory predicts that you wouldn't see any cooperation. But in reality,” claims Morris, “there's tons of cooperation around.”
For example, many microbial plankton species have jettisoned the genes needed to produce one or more essential vitamins and instead outsource them from or exchange them with other cells in their environment, says Stephen J. Giovannoni, from Oregon State University, in Corvallis. He argues that “most of the time, the fitness advantages of smaller genomes and lower cell replicating costs offset the potential fitness gains that would come from vitamin manufacture when the required nutrients are in short supply.”
As is exemplified by Prochlorococcus, extensive gene loss exists even among Cyanobacteria, a group that otherwise contains some of the most complex bacteria on Earth. But the reconstruction of archaeal genomes provides the most compelling evidence for the dominance of genome reduction and simplification in nature, according to Eugene V. Koonin and Yuri Wolf, at the National Institutes of Health's National Center for Biotechnology Information. “The pattern of gene loss and gain in archaea is not trivial; there seems to have been some net gain at the base of each major archaeal branch that was invariably followed by substantial gene loss,” they note in the journal Bioessays (doi:10.1002/bies.201300037).
Furthermore, when ancient Cyanobacteria were domesticated by the ancestors of plants, the bacteria deleted most of their genes or transferred them to the host nucleus, becoming chloroplasts, and, along with mitochondria, are considered “the ultimate realization of bacterial reductive evolution,” Koonin says. The association “dramatically increased the habitat of these photosynthetic bacteria from the sea to terrestrial ecosystems” and enabled plants to colonize the Earth, according to Ton Bisseling, at King Saud University, in Riyadh, Saudi Arabia, writing in Science (doi:10.1126/science.1256542).
Notably, though, in contrast to most other forms of microbial cooperation, BQH participants make no commitments. “At first glance, you might think that the interaction we studied involves altruism or, perhaps, some sort of reciprocal benefits. However, we know the initial state of the system, and we saw how it evolved over time in the lab. So we know the coexistence of the two [competing] bacterial types depends on the detoxification—on the protection—provided by the black queen function. Because that function is leaky, the detoxifiers can't help but produce a public good, and the beneficiaries simply take advantage of the cleaned-up environment to lose costly genes,” according to Lenski.
Giovannoni comments on the importance of “streamlining theory” to the BQH, explaining that it originally showed how gene loss works. He also notes that, although “some lost functions make interactions more complicated in ways predicted by the BQH, others enable cells to use resources more efficiently, without increasing interaction.”
“The concept of streamlining had little traction before the discovery of small-genome microbial cells in the oceans caused a shift in perceptions, putting greater emphasis on the high cost of metabolic functions in some ecosystems,” he says.
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