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Fine-scale adaptations to environmental variation and growth strategies drive phyllosphere Methylobacterium diversity

Jean-Baptiste Leducq, Émilie Seyer-Lamontagne, Domitille Condrain-Morel, Geneviève Bourret, David Sneddon, James A. Foster, Christopher J. Marx, Jack M. Sullivan, View ORCID ProfileB. Jesse Shapiro, View ORCID ProfileSteven W. Kembel
doi: https://doi.org/10.1101/2021.06.04.447128
Jean-Baptiste Leducq
1Université de Montréal
2Université du Québec à Montréal
3University of Idaho
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  • For correspondence: jeanbaptiste.leducq@gmail.com
Émilie Seyer-Lamontagne
1Université de Montréal
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Domitille Condrain-Morel
2Université du Québec à Montréal
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Geneviève Bourret
2Université du Québec à Montréal
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David Sneddon
3University of Idaho
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James A. Foster
3University of Idaho
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Christopher J. Marx
3University of Idaho
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Jack M. Sullivan
3University of Idaho
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B. Jesse Shapiro
1Université de Montréal
4McGill University
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Steven W. Kembel
2Université du Québec à Montréal
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  • ORCID record for Steven W. Kembel
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Abstract

Methylobacterium is a prevalent bacterial genus of the phyllosphere. Despite its ubiquity, little is known about the extent to which its diversity reflects neutral processes like migration and drift, or environmental filtering of life history strategies and adaptations. In two temperate forests, we investigated how phylogenetic diversity within Methylobacterium was structured by biogeography, seasonality, and growth strategies. Using deep, culture-independent barcoded marker gene sequencing coupled with culture-based approaches, we uncovered a previously underestimated diversity of Methylobacterium in the phyllosphere. We cultured very different subsets of Methylobacterium lineages depending upon the temperature of isolation and growth (20 °C or 30 °C), suggesting long-term adaptation to temperature. To a lesser extent than temperature adaptation, Methylobacterium diversity was also structured across large (>100km; between forests) and small geographical scales (<1.2km within forests), among host tree species, and was dynamic over seasons. By measuring growth of 79 isolates at different temperature treatments, we observed contrasting growth performances, with strong lineage- and season-dependent variations in growth strategies. Finally, we documented a progressive replacement of lineages with a high-yield growth strategy typical of cooperative, structured communities, in favor of those characterized by rapid growth, resulting in convergence and homogenization of community structure at the end of the growing season. Together our results show how Methylobacterium is phylogenetically structured into lineages with distinct growth strategies, which helps explain their differential abundance across regions, host tree species, and time. This works paves the way for further investigation of adaptive strategies and traits within a ubiquitous phyllosphere genus.

Abstract importance Methylobacterium is a bacterial group tied to plants. Despite its ubiquity and importance to their hosts, little is known about the processes driving Methylobacterium community dynamics. By combining traditional culture-dependent and –independent (metagenomics) approaches, we monitored Methylobacterium diversity in two temperate forests over a growing season. On the surface of tree leaves, we discovered remarkably diverse and dynamic Methylobacterium communities over short temporal (from June to October) and spatial scales (within 1.2 km). Because we cultured very different subsets of Methylobacterium diversity depending on the temperature of incubation, we suspected that these dynamics partly reflected climatic adaptation. By culturing strains in lab conditions mimicking seasonal variations, we found that diversity and environmental variations were indeed good predictors of Methylobacterium growth performances. Our findings suggest that Methylobacterium community dynamics at the surface of tree leaves results from the succession of strains with contrasted growth strategies in response to environmental variations.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/JBLED/methylo-phyllo-diversity

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Posted July 07, 2021.
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Fine-scale adaptations to environmental variation and growth strategies drive phyllosphere Methylobacterium diversity
Jean-Baptiste Leducq, Émilie Seyer-Lamontagne, Domitille Condrain-Morel, Geneviève Bourret, David Sneddon, James A. Foster, Christopher J. Marx, Jack M. Sullivan, B. Jesse Shapiro, Steven W. Kembel
bioRxiv 2021.06.04.447128; doi: https://doi.org/10.1101/2021.06.04.447128
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Fine-scale adaptations to environmental variation and growth strategies drive phyllosphere Methylobacterium diversity
Jean-Baptiste Leducq, Émilie Seyer-Lamontagne, Domitille Condrain-Morel, Geneviève Bourret, David Sneddon, James A. Foster, Christopher J. Marx, Jack M. Sullivan, B. Jesse Shapiro, Steven W. Kembel
bioRxiv 2021.06.04.447128; doi: https://doi.org/10.1101/2021.06.04.447128

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