Bacteria's Move from Sea to Land May Have Occurred Much Later Than Thought
ScienceDaily (Dec. 22, 2011) — Research by University of Tennessee, Knoxville, faculty has discovered that bacteria's move from sea to land may have occurred much later than thought. It also has revealed that the bacteria may be especially useful in bioenergy research.
Azospirillum on a plant root. (Credit: Image courtesy of University of Tennessee at Knoxville)
Igor Jouline, UT-Oak Ridge National Laboratory joint faculty professor of microbiology and researcher at ORNL's Joint Institute for Computational Sciences, performed a genome sequence analysis of the soil bacteria Azospirillum, a species' whose forebearers made the sea-to-land move. The analysis indicates the shift may have occurred only 400 million years ago, rather than approximately two billion years earlier, as originally thought.
Published in the journal PLoS Genetics, Jouline calculated the timing of the sea-land transition through studies of genome sequences of two species ofAzospirillum, a terrestrial genus with almost exclusively aquatic relatives.
Jouline conducted his research with Kristin Wuichet and Leonid Sukharnikov of the Department of Microbiology, Gladys Alexandre of Department of Biochemistry, Cellular, and Molecular Biology, and Kirill Borziak, a graduate student in the ORNL-UT Genome Science and Technology program.
"In the absence of fossil records for bacteria, it is hard to estimate when and how bacteria transitioned from sea to land," said Jouline. "Using genome sequencing and analysis of bacteria of the genus Azospirillum, which colonizes roots of important cereals and grasses, we show that these organisms transitioned from aquatic environments to land approximately at the same time that plants appeared on land -- 400 million years ago."
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Azospirillum Genomes Reveal Transition of Bacteria from Aquatic to Terrestrial Environments
Florence Wisniewski-Dyé1#, Kirill Borziak2,3#,Gurusahai Khalsa-Moyers3, Gladys Alexandre4,Leonid O. Sukharnikov2,5, Kristin Wuichet2,5,Gregory B. Hurst6, W. Hayes McDonald6¤a, Jon S. Robertson7, Valérie Barbe8, Alexandra Calteau9, Zoé Rouy9, Sophie Mangenot8, Claire Prigent-Combaret1, Philippe Normand1, Mickaël Boyer1¤b, Patricia Siguier10, Yves Dessaux11,Claudine Elmerich12, Guy Condemine13, Ganisan Krishnen14¤c, Ivan Kennedy14, Andrew H. Paterson7, Victor González15, Patrick Mavingui1,Igor B. Zhulin2,3,5,16*
1 CNRS, UMR 5557, Ecologie Microbienne, Université de Lyon, Villeurbanne, France, 2 BioEnergy Science Center, University of Tennessee–Oak Ridge National Laboratory, Oak Ridge, Tennessee, United States of America, 3 Genome Science and Technology Program, University of Tennessee–Oak Ridge National Laboratory, Oak Ridge, Tennessee, United States of America, 4 Department of Biochemistry, Cell and Molecular Biology, University of Tennessee, Knoxville, Tennessee, United States of America, 5 Department of Microbiology, University of Tennessee, Knoxville, Tennessee, United States of America, 6 Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, United States of America, 7 Plant Genome Mapping Laboratory, University of Georgia, Athens, Georgia, United States of America, 8Institut de Génomique, CEA, Génoscope, Evry, France, 9 Laboratoire d'Analyse Bioinformatique en Génomique et Métabolisme CNRS UMR8030, CEA, Génoscope, Evry, France, 10 UMR5100 Laboratoire de Microbiologie et Génétique Moléculaire, CNRS-Université Paul Sabatier, Toulouse, France, 11 Institut des Sciences du Végétal, UPR 2355, CNRS, Gif-sur-Yvette, France, 12Département de Microbiologie, BMGE, Institut Pasteur, Paris, France, 13 CNRS, UMR5240, Microbiologie Adaptation et Pathogénie, Université de Lyon, Villeurbanne, France, 14 Faculty of Agriculture, Food, and Natural Resources, The University of Sydney, Sydney, Australia, 15Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, México,16 Computer Science and Mathematics Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, United States of America
Abstract
Fossil records indicate that life appeared in marine environments ~3.5 billion years ago (Gyr) and transitioned to terrestrial ecosystems nearly 2.5 Gyr. Sequence analysis suggests that “hydrobacteria” and “terrabacteria” might have diverged as early as 3 Gyr. Bacteria of the genus Azospirillum are associated with roots of terrestrial plants; however, virtually all their close relatives are aquatic. We obtained genome sequences of two Azospirillum species and analyzed their gene origins. While most Azospirillum house-keeping genes have orthologs in its close aquatic relatives, this lineage has obtained nearly half of its genome from terrestrial organisms. The majority of genes encoding functions critical for association with plants are among horizontally transferred genes. Our results show that transition of some aquatic bacteria to terrestrial habitats occurred much later than the suggested initial divergence of hydro- and terrabacterial clades. The birth of the genus Azospirillum approximately coincided with the emergence of vascular plants on land.
Author Summary
Genome sequencing and analysis of plant-associated beneficial soil bacteriaAzospirillum spp. reveals that these organisms transitioned from aquatic to terrestrial environments significantly later than the suggested major Precambrian divergence of aquatic and terrestrial bacteria. Separation of Azospirillum from their close aquatic relatives coincided with the emergence of vascular plants on land. Nearly half of the Azospirillum genome has been acquired horizontally, from distantly related terrestrial bacteria. The majority of horizontally acquired genes encode functions that are critical for adaptation to the rhizosphere and interaction with host plants.
Citation: Wisniewski-Dyé F, Borziak K, Khalsa-Moyers G, Alexandre G, Sukharnikov LO, et al. (2011) Azospirillum Genomes Reveal Transition of Bacteria from Aquatic to Terrestrial Environments. PLoS Genet 7(12): e1002430. doi:10.1371/journal.pgen.1002430
Editor: Paul M. Richardson, Progentech, United States of America
Received: September 9, 2011; Accepted: November 2, 2011; Published: December 22, 2011
Copyright: © 2011 Wisniewski-Dyé et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported in part by grants EF-0412186, EF-0728827 (IBZ and AHP), and MCB-0622277 (GA) from the National Science Foundation and by funds from the DOE BioEnergy Science Center (IBZ) and the Genomic Science Program (GBH and WHM), which are supported by the Office of Biological and Environmental Research in the DOE Office of Science. This work was also supported by the ANR project AZORIZ (ANR-08-BLAN-0098), by the CNRS Institut Ecology et Environnement (France), and by Australian Research Council grant DP0771664 (IK and IBZ). The BioEnergy Science Center is a U.S. Department of Energy Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
* E-mail: joulineib@ornl.gov
# These authors contributed equally to this work.
¤a Current address: Vanderbilt-Ingram Cancer Center, Vanderbilt University, Nashville, Tennessee, United States of America
¤b Current address: Danone Research, Palaiseau, France
¤c Current address: Strategic Resources Research Centre, MARDI Head Quarters, Selangor, Malaysia
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