Rhizobial genetic and genomic resources for sustainable agriculture
MacLean G. Kohlmeier A * , Graham W. O’Hara A , Joshua P. Ramsay B and Jason J. Terpolilli AA
B
MacLean Kohlmeier received his PhD from the University of Manitoba in 2020 with Prof. Ivan Oresnik. He is currently a Postdoctoral Research Fellow in Microbial Genomics in the Legume Rhizobium Sciences group at Murdoch University. His research interests include gene transfer events between soil bacteria, as well as carbon metabolism and transport, and how these features affect symbiotic establishment and efficiency. |
Graham O’Hara is Director of Murdoch University’s Legume Rhizobium Sciences centre in the Food Futures Institute, and co-curator of the International Legume Inoculant Genebank (ILIG). He has worked extensively in national and international projects on applied nitrogen fixation leading to the development and dissemination of inoculant rhizobia strains. His research interest is focussed on the soil ecology, mineral nutrition, physiology and stress tolerance of rhizobia, and how this affects their performance as inoculants in the field. |
Joshua Ramsay carried out his PhD in 2004–2008 at the University of Otago with Prof. Clive Ronson. He was then a University of Cambridge Herchel Smith Postdoctoral Fellow from 2008 to 2011 and a Health Sciences Career Development Fellow at the University of Otago. Ramsay started his own lab at Curtin University in 2013. Dr Ramsay’s investigations explore the effects of mobile genetic elements in both health related and agricultural contexts. In 2018, Dr Ramsay was awarded an ARC Future Fellowship and he is currently an Associate Professor in the Curtin Medical School and Curtin Health Innovation Research Institute. |
Jason Terpolilli is Research Director of Murdoch University’s Legume Rhizobium Sciences centre in the Food Futures Institute, and co-curator of ILIG. He works closely with colleagues across Australia on several projects aimed at increasing the application of effective nitrogen-fixing rhizobia for grain and pasture legumes. His main areas of research interest are in rhizobia genetics and biochemistry and in applying genomics to develop robust approaches to studying the evolution of these organisms and their effect on farming systems in the field. |
Abstract
Rhizobia are a diverse group of α- and β-proteobacteria that boost soil fertility by forming a nitrogen-fixing symbiosis with legumes, which is why legumes are grown in rotation with cereals in agriculture. Rhizobia that naturally populate Australian soils are largely incompatible with exotic agricultural legumes, therefore, compatible strains have been imported from all over the world for use as inoculants. An amalgamated collection of these strains, called the International Legume Inoculant Genebank (ILIG), has been established at Murdoch University, to provide a centralised strain storage facility and support rhizobial research and inoculant development (see http://ilig.murdoch.edu.au). The ILIG contains 11,558 strains representing 96 bacterial species from 778 legume species collected from >1200 locations across 100 countries. New and sometimes inefficient rhizobia evolve in the field following legume inoculation, through horizontal symbiosis gene transfer from inoculants to soil bacteria. To provide a benchmark to monitor and assess the impact of this evolution, all commercial Australian inoculant strains were genome sequenced and these data made available (PRJNA783123, see https://www.ncbi.nlm.nih.gov/bioproject/PRJNA783123/). These data, and the further sequencing of the >11,000 historical strains in the ILIG, will increase our understanding of rhizobial evolution and diversity and provide the backbone for efforts to safeguard Australia’s legume inoculation program.
Keywords: horizontal gene transfer, inoculant, legume, rhizobia, sequencing, symbiosis.
MacLean Kohlmeier received his PhD from the University of Manitoba in 2020 with Prof. Ivan Oresnik. He is currently a Postdoctoral Research Fellow in Microbial Genomics in the Legume Rhizobium Sciences group at Murdoch University. His research interests include gene transfer events between soil bacteria, as well as carbon metabolism and transport, and how these features affect symbiotic establishment and efficiency. |
Graham O’Hara is Director of Murdoch University’s Legume Rhizobium Sciences centre in the Food Futures Institute, and co-curator of the International Legume Inoculant Genebank (ILIG). He has worked extensively in national and international projects on applied nitrogen fixation leading to the development and dissemination of inoculant rhizobia strains. His research interest is focussed on the soil ecology, mineral nutrition, physiology and stress tolerance of rhizobia, and how this affects their performance as inoculants in the field. |
Joshua Ramsay carried out his PhD in 2004–2008 at the University of Otago with Prof. Clive Ronson. He was then a University of Cambridge Herchel Smith Postdoctoral Fellow from 2008 to 2011 and a Health Sciences Career Development Fellow at the University of Otago. Ramsay started his own lab at Curtin University in 2013. Dr Ramsay’s investigations explore the effects of mobile genetic elements in both health related and agricultural contexts. In 2018, Dr Ramsay was awarded an ARC Future Fellowship and he is currently an Associate Professor in the Curtin Medical School and Curtin Health Innovation Research Institute. |
Jason Terpolilli is Research Director of Murdoch University’s Legume Rhizobium Sciences centre in the Food Futures Institute, and co-curator of ILIG. He works closely with colleagues across Australia on several projects aimed at increasing the application of effective nitrogen-fixing rhizobia for grain and pasture legumes. His main areas of research interest are in rhizobia genetics and biochemistry and in applying genomics to develop robust approaches to studying the evolution of these organisms and their effect on farming systems in the field. |
References
1 Fowler D et al. (2013) The global nitrogen cycle in the twenty-first century. Philos Trans R Soc Lond B Biol Sci 368, 20130164.
| Crossref | Google Scholar | PubMed |
2 Poole P et al. (2018) Rhizobia: from saprophytes to endosymbionts. Nat Rev Microbiol 16, 291-303.
| Crossref | Google Scholar | PubMed |
3 Lötjönen S, Ollikainen M (2017) Does crop rotation with legumes provide an efficient means to reduce nutrient loads and GHG emissions? Rev Agric Food Environ Stud 98, 283-312.
| Crossref | Google Scholar |
4 Smith CJ, Chalk PM (2020) Grain legumes in crop rotations under low and variable rainfall: are observed short-term N benefits sustainable? Plant Soil 453, 271-279.
| Crossref | Google Scholar |
5 Xing H et al. (2017) Incorporating grain legumes in cereal-based cropping systems to improve profitability in southern New South Wales, Australia. Agric Syst 154, 112-123.
| Crossref | Google Scholar |
8 Wang D et al. (2012) Symbiosis specificity in the legume – rhizobial mutualism. Cell Microbiol 14, 334-342.
| Crossref | Google Scholar | PubMed |
9 Allito BB et al. (2021) Legume-rhizobium specificity effect on nodulation, biomass production and partitioning of faba bean (Vicia faba L.). Sci Rep 11, 3678.
| Crossref | Google Scholar | PubMed |
10 Corbin E et al. (1977) Nodulation studies on chickpea (Cicer arietinum). Aust J Exp Agric 17, 126-134.
| Crossref | Google Scholar |
11 Howieson JG et al. (1988) Selection for acid tolerance in Rhizobium meliloti. Plant Soil 105, 179-188.
| Crossref | Google Scholar |
12 Howieson J et al. (1995) Biserrula pelecinus L.—a legume pasture species with potential for acid, duplex soils which is nodulated by unique root-nodule bacteria. Aust J Agric Res 46, 997-1009.
| Crossref | Google Scholar |
13 Finan TM et al. (2001) The complete sequence of the 1,683-kb pSymB megaplasmid from the N2-fixing endosymbiont Sinorhizobium meliloti. Proc Natl Acad Sci USA 98, 9889-9894.
| Crossref | Google Scholar | PubMed |
14 Galibert F et al. (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293, 668-672.
| Crossref | Google Scholar | PubMed |
15 Capela D et al. (2001) Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc Natl Acad Sci USA 98, 9877-9882.
| Crossref | Google Scholar | PubMed |
16 Remigi P et al. (2016) Symbiosis within symbiosis: evolving nitrogen-fixing legume symbionts. Trends Microbiol 24, 63-75.
| Crossref | Google Scholar | PubMed |
17 Sullivan JT et al. (1995) Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc Natl Acad Sci USA 92, 8985-8989.
| Crossref | Google Scholar | PubMed |
18 Ramsay JP et al. (2006) Excision and transfer of the Mesorhizobium loti R7A symbiosis island requires an integrase IntS, a novel recombination directionality factor RdfS, and a putative relaxase RlxS. Mol Microbiol 62, 723-734.
| Crossref | Google Scholar | PubMed |
19 Ramsay JP et al. (2022) An epigenetic switch activates bacterial quorum sensing and horizontal transfer of an integrative and conjugative element. Nucleic Acids Res 50, 975-988.
| Crossref | Google Scholar | PubMed |
20 Jowsey WJ et al. (2023) DUF2285 is a novel helix-turn-helix domain variant that orchestrates both activation and antiactivation of conjugative element transfer in proteobacteria. Nucleic Acids Res 51, 6841-6856.
| Crossref | Google Scholar | PubMed |
21 Nandasena KG et al. (2007) In situ lateral transfer of symbiosis islands results in rapid evolution of diverse competitive strains of mesorhizobia suboptimal in symbiotic nitrogen fixation on the pasture legume Biserrula pelecinus L. Environ Microbiol 9, 2496-2511.
| Crossref | Google Scholar | PubMed |
22 Hill Y et al. (2021) Evolution of diverse effective N2-fixing microsymbionts of Cicer arietinum following horizontal transfer of the Mesorhizobium ciceri CC1192 symbiosis integrative and conjugative element. Appl Environ Microbiol 87, e02558-20.
| Crossref | Google Scholar | PubMed |
23 Haskett TL et al. (2016) Assembly and transfer of tripartite integrative and conjugative genetic elements. Proc Natl Acad Sci USA 113, 12268-12273.
| Crossref | Google Scholar | PubMed |
24 Haskett TL et al. (2018) Sequential induction of three recombination directionality factors directs assembly of tripartite integrative and conjugative elements. PLoS Genet 14, e1007292.
| Crossref | Google Scholar | PubMed |
25 Colombi E et al. (2023) Population genomics of Australian indigenous Mesorhizobium reveals diverse nonsymbiotic genospecies capable of nitrogen-fixing symbioses following horizontal gene transfer. Microb Genom 9, 000918.
| Crossref | Google Scholar | PubMed |
26 Nandasena KG et al. (2006) Rapid in situ evolution of nodulating strains for Biserrula pelecinus L. through lateral transfer of a symbiosis island from the original mesorhizobial inoculant. Appl Environ Microbiol 72, 7365-7367.
| Crossref | Google Scholar | PubMed |
27 Elias NV, Herridge DF (2015) Naturalised populations of mesorhizobia in chickpea (Cicer arietinum L.) cropping soils: effects on nodule occupancy and productivity of commercial chickpea. Plant Soil 387, 233-249.
| Crossref | Google Scholar |
28 Howieson JG, Dilworth MJ (eds) (2016) Working with rhizobia. ACIAR Monograph Number 173. Australian Centre for International Agricultural Research, Canberra, ACT, Australia. https://www.aciar.gov.au/sites/default/files/legacy/aciar_mn_173_web-updated_31_may_2016.pdf
29 Kohlmeier MG et al. (2023) Complete genome sequence of Rhizobium leguminosarum bv. viciae SRDI969, an acid-tolerant, efficient N2-fixing microsymbiont of Vicia faba. Microbiol Resour Announc 12, e00489-00423.
| Crossref | Google Scholar | PubMed |