Group highlights
Predator/prey coevolution and microbial community-wide gene expression
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 experiments with an idealized 30-species bacterial community where we experimentally manipulated the coevolutionary history of a ciliate predator and a single bacterial prey species. Altering the coevolutionary history of the prey had little effect on the ecology of the system but induced large functional changes in community transcription and metabolic potential. These results illustrate that localized coevolutionary processes between species pairs can reverberate through ecosystem-scale transcriptional networks with important consequences for broader ecosystem function.
Hogle SL, Ruusulehto L, Cairns J, Hultman J, Hiltunen T. 2023. Localized coevolution between microbial predator and prey alters community-wide gene expression and ecosystem function. ISME J 17:514–524.
Intraspecific trait variability and species coexistence
A popular idea in ecology is that trait variation among individuals from the same species may promote the coexistence of competing species. However, theoretical and empirical tests of this idea have yielded inconsistent findings. We tested the role of intraspecific variability for the coexistence of two bacterivorous predators (a ciliate and a nemotode) using the framework of modern ecological coexistence theory. We found that variable intraspecific phenotypes promoted predator competition over niche partitioning and coexistence. This competitive outcome was driven by enhanced foraging traits (size, speed, and directionality) that increased the ciliate's fitness ratio and niche overlap with the nematode ultimately resulting in exclusion of the nematode predator.
Hogle SL‡, Hepolehto I‡, Ruokolainen L, Cairns J, Hiltunen T. 2022. Effects of phenotypic variation on consumer coexistence and prey community structure. Ecol Lett 25:307–319.
Iron scavenging by marine picocyanobacteria
The micronutrient iron limits primary productivity in at least 30% of the global ocean. However, marine picocyanobacteria are thought to avoid iron limitation due to their small cell size. We used comparative genomics, metagenomics, and machine learning methods combined with an expansive marine biogeochemical dataset to ask whether biogeographical patterns of iron scarcity can be elucidated from the genomes of the marine picocyanobacteria, which dominate the tropical and subtropical oceans. By mining this wealth of data, we identified a new organic iron metabolic pathway (siderophore uptake) in picocyanobacterial genomes and quantified it in the most abundant photosynthetic cell in the oceans, Prochlorococcus. Siderophore transporter genes are highly abundant in remote ocean areas far from terrestrial iron inputs, and their distribution is strongly negatively correlated with atmospherically deposited trace metal concentrations (Fe, Pb, Al). Our findings show that organic iron acquisition is a critical but previously unknown cyanobacterial adaptation to the global ocean's oligotrophic conditions and broadly highlights the role of iron as a selective pressure shaping the evolution of marine picocyanobacteria.
Hogle SL, Hackl T, Bundy RM, Park J, Satinsky B, Hiltunen T, Biller S, Berube PM, Chisholm SW. 2022. Siderophores as an iron source for picocyanobacteria in deep chlorophyll maximum layers of the oligotrophic ocean. ISME J 16:1636–1646.
Microbial sources of organophosphonates to the marine P cycle
Reduced organophosphonates are a major component of the marine phosphorus biogeochemical cycle, constituting over 25% of all dissolved organic phosphorus in the ocean. However, known microbial phosphonate producers are too rare to account for this amount of phosphorus in the ocean. We hypothesized that some proportion of Prochlorococcus and SAR11 cells, the two most abundant bacterioplankton in the surface ocean, must produce phosphonate compounds. Using a massive metagenomic and single-cell genomic dataset, we identified diverse bacterial and archaeal genomes containing the genes necessary for phosphonate production. These producers lack the genes required to consume and use phosphonates, implying that the ocean's sources and sinks of reduced phosphorus are partitioned into distinct microbial guilds. Importantly, we identified phosphonate biosynthesis genes in Prochlorococcus and SAR11, suggesting these dominant species contribute significantly to the global phosphonate pool. Confirming this prediction, we found that Prochlorococcus can allocate nearly 50% of cellular phosphorus towards phosphonate production in replete conditions. Extrapolating cellular phosphonate concentrations with measured cell densities, we estimated that by including Prochlorococcus and SAR11 as producers, we could easily account for the marine phosphonate pool and close the production side of the global biogeochemical budget. Our findings suggest that Prochlorococcus and SAR11 are likely major contributors to the marine phosphonate cycle.
Acker M‡, Hogle SL‡, Berube PM, Hackl T, Coe A, Stepanauskas R, Chisholm SW, Repeta DJ. 2022. Phosphonate production by marine microbes: Exploring new sources and potential function. Proc Natl Acad Sci U S A 119:e2113386119.
Phytoplankton iron limitation at marine deep chlorophyll maximum (DCM) layers
In many ocean regions, phytoplankton chlorophyll concentrations peak in distinct and persistent layers deep below the surface called subsurface chlorophyll maximum layers (SCMLs). Most biogeochemical models predict that SCMLs are formed at an optimal compensatory depth that balances nitrogen input from below and light input from above. Using shipboard incubations, metatranscriptomics, and biogeochemical proxies, we discovered unexpectedly persistent and widespread phytoplankton iron limitation (an essential micronutrient) and iron/light colimitation in SCMLs in the subtropical N. Pacific Ocean. Our results suggest that interactions and feedback between iron and light availability play an important and previously unrecognized role in controlling the productivity and biogeochemical dynamics of SCMLs in the global ocean.
Hogle SL, Dupont CL, Hopkinson BM, King AL, Buck KN, Roe KL, Stuart RK, Allen AE, Mann EL, Johnson ZI, Barbeau KA. 2018. Pervasive iron limitation at subsurface chlorophyll maxima of the California Current. Proc Natl Acad Sci U S A 115:13300–13305.