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Closely interacting microbial species pairs (e.g., predator and prey) can become coadapted via reciprocal natural selection. A fundamental challenge in evolutionary ecology is to untangle how coevolution in small species groups affects and is affected by biotic interactions in diverse communities. We conducted an experiment with a synthetic 30-species bacterial community where we experimentally manipulated the coevolutionary history of a ciliate predator and one bacterial prey species from the community. Altering the coevolutionary history of the focal prey species had little effect on community structure or carrying capacity in the presence or absence of the coevolved predator. However, community metabolic potential (represented by per-cell ATP concentration) was significantly higher in the presence of both the coevolved focal predator and prey. This ecosystem-level response was mirrored by community-wide transcriptional shifts that resulted in the differential regulation of nutrient acquisition and surface colonization pathways across multiple bacterial species. Our findings show that the disruption of localized coevolution between species pairs can reverberate through community-wide transcriptional networks even while community composition remains largely unchanged. We propose that these altered expression patterns may signal forthcoming evolutionary and ecological change.

Closely interacting microbial species pairs (e.g., predator and prey) can become coadapted via reciprocal natural selection. A fundamental challenge in evolutionary ecology is to untangle how coevolution in small species groups affects and is affected by biotic interactions in diverse communities. We conducted an experiment with a synthetic 30-species bacterial community where we experimentally manipulated the coevolutionary history of a ciliate predator and one bacterial prey species from the community. Altering the coevolutionary history of the focal prey species had little effect on community structure or carrying capacity in the presence or absence of the coevolved predator. However, community metabolic potential (represented by per-cell ATP concentration) was significantly higher in the presence of both the coevolved focal predator and prey. This ecosystem-level response was mirrored by community-wide transcriptional shifts that resulted in the differential regulation of nutrient acquisition and surface colonization pathways across multiple bacterial species. Our findings show that the disruption of localized coevolution between species pairs can reverberate through community-wide transcriptional networks even while community composition remains largely unchanged. We propose that these altered expression patterns may signal forthcoming evolutionary and ecological change.

Prochlorococcusand Synechococcusare the most abundant photosynthesizing organisms in the oceans. Gene content variation among picocyanobacterial populations in separate ocean basins often mirrors the selective pressures imposed by the region’s distinct biogeochemistry. By pairing genomic datasets with trace metal concentrations from across the global ocean, we show that the genomic capacity for siderophore-mediated iron uptake is widespread in Synechococcusand low-light adapted Prochlorococcuspopulations from deep chlorophyll maximum layers of iron-depleted regions of the oligotrophic Pacific and S. Atlantic oceans: Prochlorococcussiderophore consumers were absent in the N. Atlantic ocean (higher new iron flux) but constituted up to half of all Prochlorococcusgenomes from metagenomes in the N. Pacific (lower new iron flux). Picocyanobacterial siderophore consumers, like many other bacteria with this trait, also lack siderophore biosynthesis genes indicating that they scavenge exogenous siderophores from seawater. Statistical modeling suggests that the capacity for siderophore uptake is endemic to remote ocean regions where atmospheric iron fluxes are the smallest, especially at deep chlorophyll maximum and primary nitrite maximum layers. We argue that abundant siderophore consumers at these two common oceanographic features could be a symptom of wider community iron stress, consistent with prior hypotheses. Our results provide a clear example of iron as a selective force driving the evolution of marine picocyanobacteria.

Prochlorococcusand Synechococcusare the most abundant photosynthesizing organisms in the oceans. Gene content variation among picocyanobacterial populations in separate ocean basins often mirrors the selective pressures imposed by the region’s distinct biogeochemistry. By pairing genomic datasets with trace metal concentrations from across the global ocean, we show that the genomic capacity for siderophore-mediated iron uptake is widespread in Synechococcusand low-light adapted Prochlorococcuspopulations from deep chlorophyll maximum layers of iron-depleted regions of the oligotrophic Pacific and S. Atlantic oceans: Prochlorococcussiderophore consumers were absent in the N. Atlantic ocean (higher new iron flux) but constituted up to half of all Prochlorococcusgenomes from metagenomes in the N. Pacific (lower new iron flux). Picocyanobacterial siderophore consumers, like many other bacteria with this trait, also lack siderophore biosynthesis genes indicating that they scavenge exogenous siderophores from seawater. Statistical modeling suggests that the capacity for siderophore uptake is endemic to remote ocean regions where atmospheric iron fluxes are the smallest, especially at deep chlorophyll maximum and primary nitrite maximum layers. We argue that abundant siderophore consumers at these two common oceanographic features could be a symptom of wider community iron stress, consistent with prior hypotheses. Our results provide a clear example of iron as a selective force driving the evolution of marine picocyanobacteria.

Prochlorococcusand SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7?×?1028cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcusand SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcuson the growth of SAR11 and vice-versa, (2) whether Prochlorococcuscan meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcusis grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew 15–70% faster in co-culture with Prochlorococcus, while the growth of the latter was unaffected. When Prochlorococcuspopulations entered stationary phase, this commensal relationship rapidly became amensal, as SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria; however, the heterotrophic partner increased in abundance as Prochlorococcusdensities leveled off. The presence of Prochlorococcuswas able to meet SAR11’s central requirement for organic carbon, but not reduced sulfur. Prochlorococcusstrain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, which could be due to the production and release of glycine betaine by MIT9313, as supported by comparative genomic evidence. Our findings also suggest, but do not confirm, that ProchlorococcusMIT9313 may compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To give our results an ecological context, we assessed the relative contribution of Prochlorococcusand SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcusand SAR11 – highlighting the biogeochemical potential of these two groups.

Prochlorococcusand SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 × 1028cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcusand SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcuson the growth of SAR11 and vice-versa, (2) whether Prochlorococcuscan meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcusis grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew 15–70% faster in co-culture with Prochlorococcus, while the growth of the latter was unaffected. When Prochlorococcuspopulations entered stationary phase, this commensal relationship rapidly became amensal, as SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria; however, the heterotrophic partner increased in abundance as Prochlorococcusdensities leveled off. The presence of Prochlorococcuswas able to meet SAR11’s central requirement for organic carbon, but not reduced sulfur. Prochlorococcusstrain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, which could be due to the production and release of glycine betaine by MIT9313, as supported by comparative genomic evidence. Our findings also suggest, but do not confirm, that ProchlorococcusMIT9313 may compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To give our results an ecological context, we assessed the relative contribution of Prochlorococcusand SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcusand SAR11 – highlighting the biogeochemical potential of these two groups.