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Title: Genomes of ubiquitous marine and hypersaline Hydrogenovibrio , Thiomicrorhabdus and Thiomicrospira spp. encode a diversity of mechanisms to sustain chemolithoautotrophy in heterogeneous environments: Hydrogenovibrio, Thiomicrorhabdus, Thiomicrospira

Abstract

Chemolithoautotrophic bacteria from the genera Hydrogenovibrio, Thiomicrorhabdus and Thiomicrospira are common, sometimes dominant, isolates from sulfidic habitats including hydrothermal vents, soda and salt lakes and marine sediments. Their genome sequences confirm their membership in a deeply branching clade of the Gammaproteobacteria. Several adaptations to heterogeneous habitats are apparent. Their genomes include large numbers of genes for sensing and responding to their environment (EAL- and GGDEF-domain proteins and methyl-accepting chemotaxis proteins) despite their small sizes (2.1-3.1 Mbp). An array of sulfur-oxidizing complexes are encoded, likely to facilitate these organisms' use of multiple forms of reduced sulfur as electron donors. Hydrogenase genes are present in some taxa, including group 1d and 2b hydrogenases in Hydrogenovibrio marinus and H. thermophilus MA2-6, acquired via horizontal gene transfer. In addition to high-affinity cbb3 cytochrome c oxidase, some also encode cytochrome bd-type quinol oxidase or ba3 -type cytochrome c oxidase, which could facilitate growth under different oxygen tensions, or maintain redox balance. Carboxysome operons are present in most, with genes downstream encoding transporters from four evolutionarily distinct families, which may act with the carboxysomes to form CO2 concentrating mechanisms. These adaptations to habitat variability likely contribute to the cosmopolitan distribution of these organisms.

Authors:
ORCiD logo [1];  [1];  [1];  [1];  [2];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1] more »;  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [3];  [3];  [3];  [3];  [3];  [3];  [3];  [3];  [3];  [3];  [3];  [3];  [3];  [4];  [5];  [6] « less
  1. Department of Integrative Biology, University of South Florida, 4202 East Fowler Avenue, Tampa FL 33620 USA
  2. Biology Program, Stockton University, Galloway NJ USA
  3. Department of Energy Joint Genome Institute, Walnut Creek CA USA
  4. School of Biological & Marine Sciences, University of Plymouth, Drake Circus, Plymouth UK; Sustainable Earth Institute, University of Plymouth, Drake Circus, Plymouth UK
  5. Department of Biochemistry, University of Missouri, Columbia MO USA
  6. MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing MI USA; Department of Plant and Microbial Biology, University of California, Berkeley CA USA; MBIB Division, Lawrence Berkeley National Laboratory, Berkeley CA USA
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory-National Energy Research Scientific Computing Center (NERSC)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1529109
Alternate Identifier(s):
OSTI ID: 1432385
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Volume: 20; Journal Issue: 8; Journal ID: ISSN 1462-2912
Country of Publication:
United States
Language:
English

Citation Formats

Scott, Kathleen M., Williams, John, Porter, Cody M. B., Russel, Sydney, Harmer, Tara L., Paul, John H., Antonen, Kirsten M., Bridges, Megan K., Camper, Gary J., Campla, Christie K., Casella, Leila G., Chase, Eva, Conrad, James W., Cruz, Mercedez C., Dunlap, Darren S., Duran, Laura, Fahsbender, Elizabeth M., Goldsmith, Dawn B., Keeley, Ryan F., Kondoff, Matthew R., Kussy, Breanna I., Lane, Marannda K., Lawler, Stephanie, Leigh, Brittany A., Lewis, Courtney, Lostal, Lygia M., Marking, Devon, Mancera, Paola A., McClenthan, Evan C., McIntyre, Emily A., Mine, Jessica A., Modi, Swapnil, Moore, Brittney D., Morgan, William A., Nelson, Kaleigh M., Nguyen, Kimmy N., Ogburn, Nicholas, Parrino, David G., Pedapudi, Anangamanjari D., Pelham, Rebecca P., Preece, Amanda M., Rampersad, Elizabeth A., Richardson, Jason C., Rodgers, Christina M., Schaffer, Brent L., Sheridan, Nancy E., Solone, Michael R., Staley, Zachery R., Tabuchi, Maki, Waide, Ramond J., Wanjugi, Pauline W., Young, Suzanne, Clum, Alicia, Daum, Chris, Huntemann, Marcel, Ivanova, Natalia, Kyrpides, Nikos, Mikhailova, Natalia, Palaniappan, Krishnaveni, Pillay, Manoj, Reddy, T. B. K., Shapiro, Nicole, Stamatis, Dimitrios, Varghese, Neha, Woyke, Tanja, Boden, Rich, Freyermuth, Sharyn K., and Kerfeld, Cheryl A. Genomes of ubiquitous marine and hypersaline Hydrogenovibrio , Thiomicrorhabdus and Thiomicrospira spp. encode a diversity of mechanisms to sustain chemolithoautotrophy in heterogeneous environments: Hydrogenovibrio, Thiomicrorhabdus, Thiomicrospira. United States: N. p., 2018. Web. doi:10.1111/1462-2920.14090.
Scott, Kathleen M., Williams, John, Porter, Cody M. B., Russel, Sydney, Harmer, Tara L., Paul, John H., Antonen, Kirsten M., Bridges, Megan K., Camper, Gary J., Campla, Christie K., Casella, Leila G., Chase, Eva, Conrad, James W., Cruz, Mercedez C., Dunlap, Darren S., Duran, Laura, Fahsbender, Elizabeth M., Goldsmith, Dawn B., Keeley, Ryan F., Kondoff, Matthew R., Kussy, Breanna I., Lane, Marannda K., Lawler, Stephanie, Leigh, Brittany A., Lewis, Courtney, Lostal, Lygia M., Marking, Devon, Mancera, Paola A., McClenthan, Evan C., McIntyre, Emily A., Mine, Jessica A., Modi, Swapnil, Moore, Brittney D., Morgan, William A., Nelson, Kaleigh M., Nguyen, Kimmy N., Ogburn, Nicholas, Parrino, David G., Pedapudi, Anangamanjari D., Pelham, Rebecca P., Preece, Amanda M., Rampersad, Elizabeth A., Richardson, Jason C., Rodgers, Christina M., Schaffer, Brent L., Sheridan, Nancy E., Solone, Michael R., Staley, Zachery R., Tabuchi, Maki, Waide, Ramond J., Wanjugi, Pauline W., Young, Suzanne, Clum, Alicia, Daum, Chris, Huntemann, Marcel, Ivanova, Natalia, Kyrpides, Nikos, Mikhailova, Natalia, Palaniappan, Krishnaveni, Pillay, Manoj, Reddy, T. B. K., Shapiro, Nicole, Stamatis, Dimitrios, Varghese, Neha, Woyke, Tanja, Boden, Rich, Freyermuth, Sharyn K., & Kerfeld, Cheryl A. Genomes of ubiquitous marine and hypersaline Hydrogenovibrio , Thiomicrorhabdus and Thiomicrospira spp. encode a diversity of mechanisms to sustain chemolithoautotrophy in heterogeneous environments: Hydrogenovibrio, Thiomicrorhabdus, Thiomicrospira. United States. doi:10.1111/1462-2920.14090.
Scott, Kathleen M., Williams, John, Porter, Cody M. B., Russel, Sydney, Harmer, Tara L., Paul, John H., Antonen, Kirsten M., Bridges, Megan K., Camper, Gary J., Campla, Christie K., Casella, Leila G., Chase, Eva, Conrad, James W., Cruz, Mercedez C., Dunlap, Darren S., Duran, Laura, Fahsbender, Elizabeth M., Goldsmith, Dawn B., Keeley, Ryan F., Kondoff, Matthew R., Kussy, Breanna I., Lane, Marannda K., Lawler, Stephanie, Leigh, Brittany A., Lewis, Courtney, Lostal, Lygia M., Marking, Devon, Mancera, Paola A., McClenthan, Evan C., McIntyre, Emily A., Mine, Jessica A., Modi, Swapnil, Moore, Brittney D., Morgan, William A., Nelson, Kaleigh M., Nguyen, Kimmy N., Ogburn, Nicholas, Parrino, David G., Pedapudi, Anangamanjari D., Pelham, Rebecca P., Preece, Amanda M., Rampersad, Elizabeth A., Richardson, Jason C., Rodgers, Christina M., Schaffer, Brent L., Sheridan, Nancy E., Solone, Michael R., Staley, Zachery R., Tabuchi, Maki, Waide, Ramond J., Wanjugi, Pauline W., Young, Suzanne, Clum, Alicia, Daum, Chris, Huntemann, Marcel, Ivanova, Natalia, Kyrpides, Nikos, Mikhailova, Natalia, Palaniappan, Krishnaveni, Pillay, Manoj, Reddy, T. B. K., Shapiro, Nicole, Stamatis, Dimitrios, Varghese, Neha, Woyke, Tanja, Boden, Rich, Freyermuth, Sharyn K., and Kerfeld, Cheryl A. Fri . "Genomes of ubiquitous marine and hypersaline Hydrogenovibrio , Thiomicrorhabdus and Thiomicrospira spp. encode a diversity of mechanisms to sustain chemolithoautotrophy in heterogeneous environments: Hydrogenovibrio, Thiomicrorhabdus, Thiomicrospira". United States. doi:10.1111/1462-2920.14090. https://www.osti.gov/servlets/purl/1529109.
@article{osti_1529109,
title = {Genomes of ubiquitous marine and hypersaline Hydrogenovibrio , Thiomicrorhabdus and Thiomicrospira spp. encode a diversity of mechanisms to sustain chemolithoautotrophy in heterogeneous environments: Hydrogenovibrio, Thiomicrorhabdus, Thiomicrospira},
author = {Scott, Kathleen M. and Williams, John and Porter, Cody M. B. and Russel, Sydney and Harmer, Tara L. and Paul, John H. and Antonen, Kirsten M. and Bridges, Megan K. and Camper, Gary J. and Campla, Christie K. and Casella, Leila G. and Chase, Eva and Conrad, James W. and Cruz, Mercedez C. and Dunlap, Darren S. and Duran, Laura and Fahsbender, Elizabeth M. and Goldsmith, Dawn B. and Keeley, Ryan F. and Kondoff, Matthew R. and Kussy, Breanna I. and Lane, Marannda K. and Lawler, Stephanie and Leigh, Brittany A. and Lewis, Courtney and Lostal, Lygia M. and Marking, Devon and Mancera, Paola A. and McClenthan, Evan C. and McIntyre, Emily A. and Mine, Jessica A. and Modi, Swapnil and Moore, Brittney D. and Morgan, William A. and Nelson, Kaleigh M. and Nguyen, Kimmy N. and Ogburn, Nicholas and Parrino, David G. and Pedapudi, Anangamanjari D. and Pelham, Rebecca P. and Preece, Amanda M. and Rampersad, Elizabeth A. and Richardson, Jason C. and Rodgers, Christina M. and Schaffer, Brent L. and Sheridan, Nancy E. and Solone, Michael R. and Staley, Zachery R. and Tabuchi, Maki and Waide, Ramond J. and Wanjugi, Pauline W. and Young, Suzanne and Clum, Alicia and Daum, Chris and Huntemann, Marcel and Ivanova, Natalia and Kyrpides, Nikos and Mikhailova, Natalia and Palaniappan, Krishnaveni and Pillay, Manoj and Reddy, T. B. K. and Shapiro, Nicole and Stamatis, Dimitrios and Varghese, Neha and Woyke, Tanja and Boden, Rich and Freyermuth, Sharyn K. and Kerfeld, Cheryl A.},
abstractNote = {Chemolithoautotrophic bacteria from the genera Hydrogenovibrio, Thiomicrorhabdus and Thiomicrospira are common, sometimes dominant, isolates from sulfidic habitats including hydrothermal vents, soda and salt lakes and marine sediments. Their genome sequences confirm their membership in a deeply branching clade of the Gammaproteobacteria. Several adaptations to heterogeneous habitats are apparent. Their genomes include large numbers of genes for sensing and responding to their environment (EAL- and GGDEF-domain proteins and methyl-accepting chemotaxis proteins) despite their small sizes (2.1-3.1 Mbp). An array of sulfur-oxidizing complexes are encoded, likely to facilitate these organisms' use of multiple forms of reduced sulfur as electron donors. Hydrogenase genes are present in some taxa, including group 1d and 2b hydrogenases in Hydrogenovibrio marinus and H. thermophilus MA2-6, acquired via horizontal gene transfer. In addition to high-affinity cbb3 cytochrome c oxidase, some also encode cytochrome bd-type quinol oxidase or ba3 -type cytochrome c oxidase, which could facilitate growth under different oxygen tensions, or maintain redox balance. Carboxysome operons are present in most, with genes downstream encoding transporters from four evolutionarily distinct families, which may act with the carboxysomes to form CO2 concentrating mechanisms. These adaptations to habitat variability likely contribute to the cosmopolitan distribution of these organisms.},
doi = {10.1111/1462-2920.14090},
journal = {Environmental Microbiology},
number = 8,
volume = 20,
place = {United States},
year = {2018},
month = {4}
}

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