Host control over ineffective (non fixing) rhizobial symbionts

Host control mechanisms are thought to be critical for selecting against ineffective mutants in symbiont populations. In rhizobia, non-fixing strains are common and these ineffective symbionts are predicted to destabilize the interaction. Some of our recent research has tested a legume host’s ability to constrain the infection and proliferation of a native ineffective rhizobial strains. Lotus strigosus hosts were experimentally inoculated with pairs of Bradyrhizobium strains that naturally vary in symbiotic benefit, including a cheater symbiont strain that proliferates in the roots of singly-infected hosts yet provides zero growth benefits. Within coinfected hosts, the cheaters (and other ineffective strains) exhibited lower infection rates than competing beneficial strains and grew to smaller population sizes within those nodules. In vitro assays revealed that infection-rate differences among  competing strains were not due to variation in rhizobial growth rate or inter-strain toxicity. These results can explain how a rapidly growing cheater symbiont – that exhibits a massive fitness advantage in single infections – can be prevented from sweeping through a beneficial population of symbionts.

Regus, J. U., K.A. Gano,  Holllowell, A.C.,  V. Sofish, J. L. Sachs . Lotus hosts delimit the mutualism-parasitism continuum of Bradyrhizobium   2015  Journal of Evolutionary Biology. 28, 447-458 [PDF]

Regus, J. U., Gano, K. A., Hollowell, A. C., Sachs, J. L. Efficiency of partner choice and sanctions in Lotus is not altered by nitrogen fertilization   2014 Proceedings of the Royal Society of London. 281, 20132587 [PDF]

Sachs, J.L., Russell, J. E., Lii, Y. E., Black, K. C., Lopez, G., and Patil, A. S. 2010. Host control over infection and proliferation of a cheater symbiont. Journal of Evolutionary Biology. 23:1919-1927. [PDF]

Simms, E. L., Taylor, D. L., Povich, J., Shefferson, R. P., Sachs, J. L., Urbina, M., and Tauszick, Y. 2006. An empirical test of partner choice mechanisms in a wild legume- rhizobium interaction. Proceedings of the Royal Society of London 273:77-81.[PDF]

The evolution of uncooperative symbionts
A key prediction for symbioses is that they are evolutionarily unstable: mutants are predicted to arise and spread in symbiont populations that exploit host resources without paying costs to hosts. For instance, rhizobia are bacteria that fix nitrogen in legume roots in exchange for photosynthates from their hosts. Uncooperative rhizobia – including non-fixing and non-nodulating strains – appear common in agriculture, yet their population biology and origins remain unknown in natural soils. In a recent study (Sachs et al. 2010a, below), a phylogenetically broad sample of 62 wild-collected rhizobial isolates was experimentally inoculated onto Lotus strigosus to assess their nodulation ability and effects on host growth.
A cheater strain was discovered that proliferated in host tissue while offering no benefit; its fitness was superior to that of beneficial strains. Phylogenetic reconstruction of Bradyrhizobium rDNA and transmissible symbiosis-island loci suggest that the cheater evolved via a massive symbiotic gene transfer event. Many non-nodulating strains were also identified and it appears that nodulation ability has been recurrently lost in the symbiont population.
Sachs, J.L., Ehinger, E. O., & Simms, E. L. 2010a.  Origins of cheating and loss of symbiosis in wild Bradyrhizobium. Journal of Evolutionary Biology. 23:1075-1089. [PDF]
Sachs, J. L., and Simms, E.L. 2008. The origins of uncooperative rhizobia. Oikos117:961-966. [PDF]
Sachs, J. L., and Simms, E.L. 2006. Pathways to mutualism breakdown. Trends in Ecology and Evolution 21:585-592 [PDF]
Sachs, J. L. and Wilcox, T.P. 2006. A shift to parasitism in the jellyfish symbiont Symbiodinium microadtriaticum. Proceedings of the Royal Society of London, B. 273:425-429. [PDF]

Evolutionary origins and stability of symbiosis

Bacterial symbioses range from short-term interactions to bacterial-derived organelles and endosymbionts. Despite the importance and near ubiquity of these beneficial infections, key questions about evolution of bacterial symbioses remain unanswered. One fundamental problem is to resolve the origins of symbiotic traits in bacteria. Originally, theoreticians predicted that pathogenic bacteria often undergo transitions into commensal or beneficial partners. More recently biologists have used genomic data to argue that parasites and symbionts must represent independent origins (of host association) because genetic constraints hinder transitions between these states. A related problem is to test hypotheses about the evolutionary robustness of bacterial symbioses. Cooperation models predict that faster-evolving microbes are selected to exploit eukaryotic hosts (hence that parasitic mutants can fix in symbiont populations). Nonetheless studies of bacterial lineages have rarely studied transition rates between symbiosis and parasitism or examined the stability of bacterial cooperation over deep time. 

Sachs, J. L. and Bull, J.J. 2005. Experimental evolution of conflict mediation between genomes Proceedings of the National Academy of Sciences 102:390-395. [PDF]

Medina, M. and Sachs, J.L. 2010. Symbiont genomics; Our new tangled bank. Genomics 95:129-137. [PDF]

Sachs, J. L., Essenberg, C. and Turcotte. M. M. 2011 New Paradigms for the evolution of beneficial infections. Trends in Ecology and Evolution. 26: 202-209. [PDF]

Sachs, J. L., Russell, J. E. and Hollowell, A. C. 2011. Evolutionary instability of symbiotic

function in Bradyrhizobium. PLoS One 6: e26370. [PDF]

 Sachs, J.L., Skophammer, R.G., and Regus, J.U. 2011. Evolutionary transitions in bacterial symbiosis. Proceedings of the National Academy of Sciences USA. 108: 10800-10807. [PDF]

Sachs, J. L., Skophammer, R.G., and Stajich, J. E. 2014. Evolutionary origins and diversification of proteobacterial mutualists. Proceedings of the Royal Society B. 281:20132146 [PDF]




Microecology of rhizosphere bacteria

Rhizosphere bacteria often encounter multiple plant hosts and diverse environmental pressures in the soil and can exhibit multiple life histories including host-inhabiting and free-living stages. Research on rhizosphere bacteria -- including pathogens and beneficial symbionts that inhabit plant roots -- has primarily focused on infection of hosts. In the mean time, key questions about the ecology and evolution of free-living stages has remained unanswered. For instance, is host association ubiquitous within bacterial lineages, or do host-infecting genotypes represent subsets of free-living populations? Assuming that host infection and free-living existence exert different selective pressures, do diverged bacterial lineages result? Another set of questions addresses the traits that favor the spread of some strains over others in rhizosphere populations. One of the traits that appears to be particularly important is multidrug resistance. 

Hollowell, A.C., K.A. Gano, G. Lopez, K. Shahin, J. U. Regus, N. Gleason, S. Greater, V. Pahua, J. L. Sachs. 2015 Native California soils are selective reservoirs for multidrug resistant bacteria  Environmental Microbiology Reports. 7,442-449 [PDF]

 Sachs, J.L., Kembel, S.W., Lau, A.H., and Simms, E.L.  2009. In situ phylogenetic structure and diversity of wild Bradyrhizobium communities. Applied and Environmental Microbiology 75: 4727-4735. [PDF]