Dormancy dampens the microbial distance-decay relationship

Kj, Locey; Muscarella, Mario E.; Larsen, Megan L.; Bray, S R; Jones, SE; Lennon, Jay T

doi:10.1101/717546

Cited by 25 publications

(29 citation statements)

References 54 publications

(70 reference statements)

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“…While mutation accumulation and fluctuation in genotype frequencies under LTSP strongly suggest that cells do replicate under LTSP, it is quite reasonable to predict that LTSP cells may also spend substantial fractions of time under dormancy. Such dormancy may shield cells from the selection, thus permitting the maintenance of variants that are not currently favored ( 34 ). More study is needed to investigate dormancy under LTSP and its effect on the maintenance of genetic variation.…”

Section: Discussionmentioning

confidence: 99%

Adaptations Accumulated under Prolonged Resource Exhaustion Are Highly Transient

Avrani

Katz²,

Hershberg³

2020

mSphere

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Many nonsporulating bacterial species can survive for years within exhausted growth media in a state termed long-term stationary phase (LTSP). We have been carrying out evolutionary experiments aimed at elucidating the dynamics of genetic adaptation under LTSP. We showed that Escherichia coli adapts to prolonged resource exhaustion through the highly convergent acquisition of mutations. In the most striking example of such convergent adaptation, we observed that across all independently evolving LTSP populations, over 90% of E. coli cells carry mutations to one of three specific sites of the RNA polymerase core enzyme (RNAPC). These LTSP adaptations reduce the ability of the cells carrying them to grow once fresh resources are again provided. Here, we examine how LTSP populations recover from costs associated with their adaptation once resources are again provided to them. We demonstrate that due to the ability of LTSP populations to maintain high levels of standing genetic variation during adaptation, costly adaptations are very rapidly purged from the population once they are provided with fresh resources. We further demonstrate that recovery from costs acquired during adaptation under LTSP occurs more rapidly than would be possible if LTSP adaptations had fixed during the time populations spent under resource exhaustion. Finally, we previously reported that under LTSP, some clones develop a mutator phenotype, greatly increasing their mutation accumulation rates. Here, we show that the mechanisms by which populations recover from costs associated with fixed adaptations may depend on mutator status. IMPORTANCE Many bacterial species can survive for decades under starvation, following the exhaustion of external growth resources. We have previously shown that bacteria genetically adapt under these conditions in a manner that reduces their ability to grow once resources again become available. Here, we study how populations that have been subject to very prolonged resource exhaustion recover from costs associated with their adaptation. We demonstrate that rapid adaptations acquired under prolonged starvation tend to be highly transient, rapidly reducing in frequency once bacteria are no longer starved. Our results shed light on the longer-term consequences of bacterial survival under prolonged starvation. More generally, these results may also be applicable to understanding longer-term consequences of rapid adaptation to additional conditions as well.

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Section: Discussionmentioning

confidence: 99%

Adaptations Accumulated under Prolonged Resource Exhaustion Are Highly Transient

Avrani

Katz²,

Hershberg³

2020

mSphere

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“…We characterized composition of the active and total portions of the bacterial communities by sequencing 16S rRNA genes (DNA) and transcripts (RNA), respectively. While sequences recovered from the DNA pool can come from active or inactive individuals, sequences from the RNA pool are commonly used to make inferences about active microorganisms given that rRNA transcripts have short half‐lives and that ribosomes are required by cells for protein synthesis (Molin and Givskov , Bowsher et al , Locey et al , Steiner et al ). Sequences were processed in mothur (v. 1.41.1; Schloss et al ) and 97% similar operational taxonomic units (OTUs) were created using the OptiClust algorithm (Westcott and Schloss ).…”

Section: Methodsmentioning

confidence: 99%

“…Many bacteria have evolved persistence strategies (e.g., spores, cysts, resting stages, slow growth) that buffer against harsh environmental transitions, such as those encountered when dispersed along terrestrial‐aquatic flow paths (Barcina et al , Lennon and Jones ). By weakening the strength of species sorting, these persistence strategies may increase the apparent similarity between terrestrial and aquatic bacterial communities (Nemergut et al , Locey et al , Wisnoski et al ), especially when techniques are used that lend equal weight to active, slow‐growing, and dormant bacteria (e.g., DNA‐based methods). As a result, the importance of terrestrial‐derived bacteria in aquatic community assembly may not be fully understood when inferred from diversity patterns that do not explicitly consider the metabolic heterogeneity that exists within bacterial communities.…”

Section: Introductionmentioning

confidence: 99%

Metabolic insight into bacterial community assembly across ecosystem boundaries

Wisnoski

Muscarella

Larsen

et al. 2020

Ecology

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The movement of organisms across habitat boundaries has important consequences for populations, communities, and ecosystems. However, because most species are not well adapted to all habitat types, dispersal into suboptimal habitats could induce physiological changes associated with persistence strategies that influence community assembly. For example, high rates of cross‐boundary dispersal are thought to maintain sink populations of terrestrial bacteria in aquatic habitats, but these bacteria may also persist by lowering their metabolic activity, introducing metabolic heterogeneity that buffers the population against species sorting. To differentiate between these assembly processes, we analyzed bacterial composition along a hydrological flow path from terrestrial soils through an aquatic reservoir by sequencing the active and total (active + inactive) portions of the community. When metabolic heterogeneity was ignored, our data were consistent with views that cross‐boundary dispersal is important for structuring aquatic bacterial communities. In contrast, we found evidence for strong species sorting in the active portion of the aquatic community, suggesting that dispersal may have a weaker effect than persistence strategies on aquatic community assembly. By accounting for metabolic heterogeneity in complex communities, our findings clarify the roles of local‐ and regional‐scale assembly processes in terrestrial‐aquatic meta‐ecosystems.

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“…Several hypotheses have been put forward to explain these observations ( 38 , 39 ). Primarily, bacteria are thought to be able to maintain wide geographic ranges in the face of environmental variation by entering dormant states ( 39 , 40 ), leading to limited geographic turnover and shallow taxon-area curves ( 15 , 28 , 41 ). However, methodological artifacts may also account for some observations of weak spatial differences ( 28 ).…”

Section: Introductionmentioning

confidence: 99%

Soil Bacterial Communities Exhibit Strong Biogeographic Patterns at Fine Taxonomic Resolution

et al. 2020

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Bacteria have been inferred to exhibit relatively weak biogeographic patterns. To what extent such findings reflect true biological phenomena or methodological artifacts remains unclear. Here, we addressed this question by analyzing the turnover of soil bacterial communities from three data sets. We applied three methodological innovations: (i) design of a hierarchical sampling scheme to disentangle environmental from spatial factors driving turnover; (ii) resolution of 16S rRNA gene amplicon sequence variants to enable higher-resolution community profiling; and (iii) application of the new metric zeta diversity to analyze multisite turnover and drivers. At fine taxonomic resolution, rapid compositional turnover was observed across multiple spatial scales. Turnover was overwhelmingly driven by deterministic processes and influenced by the rare biosphere. The communities also exhibited strong distance decay patterns and taxon-area relationships, with z values within the interquartile range reported for macroorganisms. These biogeographical patterns were weakened upon applying two standard approaches to process community sequencing data: clustering sequences at 97% identity threshold and/or filtering the rare biosphere (sequences lower than 0.05% relative abundance). Comparable findings were made across local, regional, and global data sets and when using shotgun metagenomic markers. Altogether, these findings suggest that bacteria exhibit strong biogeographic patterns, but these signals can be obscured by methodological limitations. We advocate various innovations, including using zeta diversity, to advance the study of microbial biogeography. IMPORTANCE It is commonly thought that bacterial distributions show lower spatial variation than for multicellular organisms. In this article, we present evidence that these inferences are artifacts caused by methodological limitations. Through leveraging innovations in sampling design, sequence processing, and diversity analysis, we provide multifaceted evidence that bacterial communities in fact exhibit strong distribution patterns. This is driven by selection due to factors such as local soil characteristics. Altogether, these findings suggest that the processes underpinning diversity patterns are more unified across all domains of life than previously thought, which has broad implications for the understanding and management of soil biodiversity.

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Dormancy dampens the microbial distance-decay relationship

Abstract: 1 2 1 3

Cited by 25 publications

References 54 publications

Adaptations Accumulated under Prolonged Resource Exhaustion Are Highly Transient

Adaptations Accumulated under Prolonged Resource Exhaustion Are Highly Transient

Metabolic insight into bacterial community assembly across ecosystem boundaries

Soil Bacterial Communities Exhibit Strong Biogeographic Patterns at Fine Taxonomic Resolution

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