Tracking contemporary microbial evolution in a changing ocean

Brennan, Georgina; Logares, Ramiro

doi:10.1016/j.tim.2022.09.001

Cited by 12 publications

(22 citation statements)

References 74 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…After training, the classifier was applied to all 263 species above the abundance cutoff. Gradual change was identified if a linear fit to the daily linearly interpolated distances, excluding dates closer than a month to the starting date, resulted in an adjusted R 2 of at least 0.55. Dates closer than a month to the starting date were excluded because they tended to be highly similar, and a linear interpolation was applied to account for uneven sampling dates, particularly the high frequency of summer sampling in the latter decade of the timeseries.…”

Section: Methodsmentioning

confidence: 99%

“…Although microbial ecology has blossomed into a rich field spanning experimental and natural systems, our understanding of microbial evolution relies primarily on phylogenetic reconstructions and laboratory experiments. Phylogenies provide insight into ancient evolutionary events 1 , but lack insight into contemporary evolution 2 that occurs on directly observable time scales. Laboratory approaches, such as the E. coli long-term evolution experiment 3 , are able to directly observe evolutionary processes, but lack the context of complex communities typical of natural environments.…”

Section: Main Textmentioning

confidence: 99%

See 1 more Smart Citation

Bacterial ecology and evolution converge on seasonal and decadal scales

Rohwer,

Kirkpatrick,

Garcia

et al. 2024

Preprint

View full text Add to dashboard Cite

Ecology and evolution are distinct theories, but the short lifespans and large population sizes of microbes allow evolution to unfold along contemporary ecological time scales. To document this in a natural system, we collected a two-decade, 471-metagenome time series from a single site in a freshwater lake, which we refer to as the TYMEFLIES dataset. This massive sampling and sequencing effort resulted in the reconstruction of 30,389 metagenomic-assembled genomes (MAGs) over 50% complete, which dereplicated into 2,855 distinct genomes (>96% nucleotide sequence identity). We found both ecological and evolutionary processes occurred at seasonal time scales. There were recurring annual patterns at the species level in abundances, nucleotide diversities (π), and single nucleotide variant (SNV) profiles for the majority of all taxa. During annual blooms, we observed both higher and lower nucleotide diversity, indicating that both ecological differentiation and competition drove evolutionary dynamics. Overlayed upon seasonal patterns, we observed long-term change in 20% of the species’ SNV profiles including gradual changes, step changes, and disturbances followed by resilience. Most abrupt changes occurred in a single species, suggesting evolutionary drivers are highly specific. Nevertheless, seven members of the abundantNanopelagicaceaefamily experienced abrupt change in 2012, an unusually hot and dry year. This shift coincided with increased numbers of genes under selection involved in amino acid and nucleic acid metabolism, suggesting fundamental organic nitrogen compounds drive strain differentiation in the most globally abundant freshwater family. Overall, we observed seasonal and decadal trends in both interspecific ecological and intraspecific evolutionary processes. The convergence of microbial ecology and evolution on the same time scales demonstrates that understanding microbiomes requires a new unified approach that views ecology and evolution as a single continuum.

show abstract

Section: Methodsmentioning

confidence: 99%

Section: Main Textmentioning

confidence: 99%

Bacterial ecology and evolution converge on seasonal and decadal scales

Rohwer,

Kirkpatrick,

Garcia

et al. 2024

Preprint

View full text Add to dashboard Cite

show abstract

“…These shifts might not necessarily alter the species’ realized niche [ 40 ] and could be interpreted as one of the mechanisms of microbial species to cope with environmental variation. However, when the environmental variations surpass the limits of adaptability provided by the species' microdiversity, adaptive evolution could be initiated through TO or TA [ 40 , 45 , 46 ]. Therefore, comprehending the existing microdiversity within marine microbes is crucial not only for assessing a species’ potential adaptability to environmental changes but also for tracking the ongoing shifts in variant distribution driven by evolving niches.…”

Section: Ocean Microbes Are Key For the Functioning Of The Earth's Sy...mentioning

confidence: 99%

“…Understanding microbial microdiversity in the ocean represents a critical challenge for the coming years. Increasing knowledge within this field will yield important insights into microbial spatiotemporal distributions [ 40 , 47 – 53 ], ecological interactions [ 54 , 55 ], ecosystem function and its maintenance in fluctuating environments [ 49 , 56 – 58 ], and the species’ reactions to changing niches due to climate change [ 43 , 45 , 46 , 49 ]. Currently, only a few studies investigating the impact of climate change on microbial distributions have taken into account microdiversity and adaptative mechanisms [ 43 , 46 , 49 , 59 ].…”

Section: Ocean Microbes Are Key For the Functioning Of The Earth's Sy...mentioning

confidence: 99%

Decoding populations in the ocean microbiome

Logares

2024

Microbiome

Self Cite

View full text Add to dashboard Cite

Understanding the characteristics and structure of populations is fundamental to comprehending ecosystem processes and evolutionary adaptations. While the study of animal and plant populations has spanned a few centuries, microbial populations have been under scientific scrutiny for a considerably shorter period. In the ocean, analyzing the genetic composition of microbial populations and their adaptations to multiple niches can yield important insights into ecosystem function and the microbiome's response to global change. However, microbial populations have remained elusive to the scientific community due to the challenges associated with isolating microorganisms in the laboratory. Today, advancements in large-scale metagenomics and metatranscriptomics facilitate the investigation of populations from many uncultured microbial species directly from their habitats. The knowledge acquired thus far reveals substantial genetic diversity among various microbial species, showcasing distinct patterns of population differentiation and adaptations, and highlighting the significant role of selection in structuring populations. In the coming years, population genomics is expected to significantly increase our understanding of the architecture and functioning of the ocean microbiome, providing insights into its vulnerability or resilience in the face of ongoing global change.

show abstract

“…The annotated texts in each panel indicate the significance of the main and interaction effects of experimental evolution environment and assay environment (asterisks indicate significant effects, and 'ns' non-significant effects), with detailed statistics provided in Table S1. versity (Dobzhansky, 1950;Fischer, 1960;Pianka, 1966;Puurtinen et al, 2016;Stevens, 1989), as well as the potential of evolutionary adaptation under future climate changes (Brennan & Logares, 2023;Hoffmann & Sgrò, 2011;Kelly, 2019;McGaughran et al, 2021;Shaw & Etterson, 2012). A recent study distinguished between two scenarios of temperature dependence in mutational effects (Chu et al, 2020; see graphical abstract related to this article), here referred to as 'more beneficial mutations' and 'stronger beneficial mutation effects' at warmer temperatures.…”

Section: F I G U R Ementioning

confidence: 99%

Linking temperature dependence of fitness effects of mutations to thermal niche adaptation

Chen,

Zhang

2023

Journal of Evolutionary Biology

View full text Add to dashboard Cite

Fitness effects of mutations may generally depend on temperature that influences all rate‐limiting biophysical and biochemical processes. Earlier studies suggested that high temperatures may increase the availability of beneficial mutations (‘more beneficial mutations’), or allow beneficial mutations to show stronger fitness effects (‘stronger beneficial mutation effects’). The ‘more beneficial mutations’ scenario would inevitably be associated with increased proportion of conditionally beneficial mutations at higher temperatures. This in turn predicts that populations in warm environments show faster evolutionary adaptation but suffer fitness loss when faced with cold conditions, and those evolving in cold environments become thermal‐niche generalists (‘hotter is narrower’). Under the ‘stronger beneficial mutation effects’ scenario, populations evolving in warm environments would show faster adaptation without fitness costs in cold environments, leading to a ‘hotter is (universally) better’ pattern in thermal niche adaptation. We tested predictions of the two competing hypotheses using an experimental evolution study in which populations of two model bacterial species, Escherichia coli and Pseudomonas fluorescens, evolved for 2400 generations at three experimental temperatures. Results of reciprocal transplant experiments with our P. fluorescens populations were largely consistent with the ‘hotter is narrower’ prediction. Results from the E. coli populations clearly suggested stronger beneficial mutation effects at higher assay temperatures, but failed to detect faster adaptation in populations evolving in warmer experimental environments (presumably because of limitation in the supply of genetic variation). Our results suggest that the influence of temperature on mutational effects may provide insight into the patterns of thermal niche adaptation and population diversification across thermal conditions.

show abstract

Tracking contemporary microbial evolution in a changing ocean

Cited by 12 publications

References 74 publications

Bacterial ecology and evolution converge on seasonal and decadal scales

Bacterial ecology and evolution converge on seasonal and decadal scales

Decoding populations in the ocean microbiome

Linking temperature dependence of fitness effects of mutations to thermal niche adaptation

Contact Info

Product

Resources

About