The social amoeba Dictyostelium discoideum engages in a complex relationship with bacterial endosymbionts in the genus Paraburkholderia, which can benefit their host by imbuing it with the ability to carry prey bacteria throughout its life cycle. The relationship between D. discoideum and Paraburkholderia has been shown to take place across many strains and a large geographical area, but little is known about Paraburkholderia’s potential interaction with other dictyostelid species. We explore the ability of three Paraburkholderia species to stably infect and induce bacterial carriage in other dictyostelid hosts. We found that all three Paraburkholderia species successfully infected and induced carriage in seven species of Dictyostelium hosts. While the overall behaviour was qualitatively similar to that previously observed in infections of D. discoideum, differences in the outcomes of different host/symbiont combinations suggest a degree of specialization between partners. Paraburkholderia was unable to maintain a stable association with the more distantly related host Polysphondylium violaceum. Our results suggest that the mechanisms and evolutionary history of Paraburkholderia’s symbiotic relationships may be general within Dictyostelium hosts, but not so general that it can associate with hosts of other genera. Our work further develops an emerging model system for the study of symbiosis in microbes.
more »
« less
Symbiotic bacteria, immune-like sentinel cells, and the response to pathogens in a social amoeba
Some endosymbionts living within a host must modulate their hosts’ immune systems in order to infect and persist. We studied the effect of a bacterial endosymbiont on a facultatively multicellular social amoeba host. Aggregates of the amoeba Dictyostelium discoideum contain a subpopulation of sentinel cells that function akin to the immune systems of more conventional multicellular organisms. Sentinel cells sequester and discard toxins from D. discoideum aggregates and may play a central role in defence against pathogens. We measured the number and functionality of sentinel cells in aggregates of D. discoideum infected by bacterial endosymbionts in the genus Paraburkholderia. Infected D. discoideum produced fewer and less functional sentinel cells, suggesting that Paraburkholderia may interfere with its host’s immune system. Despite impaired sentinel cells, however, infected D. discoideum were less sensitive to ethidium bromide toxicity, suggesting that Paraburkholderia may also have a protective effect on its host. By contrast, D. discoideum infected by Paraburkholderia did not show differences in their sensitivity to two non-symbiotic pathogens. Our results expand previous work on yet another aspect of the complicated relationship between D. discoideum and Paraburkholderia, which has considerable potential as a model for the study of symbiosis.
more »
« less
- PAR ID:
- 10468931
- Publisher / Repository:
- Royal Society Open Science
- Date Published:
- Journal Name:
- Royal Society Open Science
- Volume:
- 10
- Issue:
- 8
- ISSN:
- 2054-5703
- Subject(s) / Keyword(s):
- sentinel cells, symbiosis, pathogens, Dictyostelium, Paraburkholderia
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Bacterial endosymbionts can provide benefits for their eukaryotic hosts, but it is often unclear if endosymbionts benefit from these relationships. The social amoeba Dictyostelium discoideum associates with three species of Paraburkholderia endosymbionts, including P. agricolaris and P. hayleyella. These endosymbionts can be costly to the host but are beneficial in certain contexts because they allow D. discoideum to carry prey bacteria through the dispersal stage. In experiments where no other species are present, P. hayleyella benefits from D. discoideum while P. agricolaris does not. However, the presence of other species may influence this symbiosis. We tested if P. agricolaris and P. hayleyella benefit from D. discoideum in the context of resource competition with Klebsiella pneumoniae, the typical laboratory prey of D. discoideum. Without D. discoideum, K. pneumoniae depressed the growth of both Paraburkholderia symbionts, consistent with competition. P. hayleyella was more harmed by interspecific competition than P. agricolaris. We found that P. hayleyella was rescued from competition by D. discoideum, while P. agricolaris was not. This may be because P. hayleyella is more specialized as an endosymbiont; it has a highly reduced genome compared to P. agricolaris and may have lost genes relevant for resource competition outside of its host.more » « less
-
The evolution of symbiotic interactions may be affected by unpredictable conditions. However, a link between prevalence of these conditions and symbiosis has not been widely demonstrated. We test for these associations usingDictyostelium discoideumsocial amoebae and their bacterial endosymbionts.D. discoideumcommonly hosts endosymbiotic bacteria from three taxa:Paraburkholderia, Amoebophilusand Chlamydiae. Three species of facultativeParaburkholderiaendosymbionts are the best studied and give hosts the ability to carry prey bacteria through the dispersal stage to new environments.Amoebophilusand Chlamydiae are obligate endosymbiont lineages with no measurable impact on host fitness. We tested whether the frequency of both single infections and coinfections of these symbionts were associated with the unpredictability of their soil environments by using symbiont presence-absence data fromD. discoideumisolates from 21 locations across the eastern United States. We found that symbiosis across all infection types, symbiosis withAmoebophilusand Chlamydiae obligate endosymbionts, and symbiosis involving coinfections were not associated with any of our measures. However, unpredictable precipitation was associated with symbiosis in two species ofParaburkholderia, suggesting a link between unpredictable conditions and symbiosis.more » « less
-
Symbiotic interactions may change depending on third parties like predators or prey. Third-party interactions with prey bacteria are central to the symbiosis betweenDictyostelium discoideumsocial amoeba hosts andParaburkholderiabacterial symbionts. Symbiosis with inedibleParaburkholderiaallows hostD. discoideumto carry prey bacteria through the dispersal stage where hosts aggregate and develop into fruiting bodies that disperse spores. Carrying prey bacteria benefits hosts when prey are scarce but harms hosts when prey bacteria are plentiful, possibly because hosts leave some prey bacteria behind while carrying. Thus, understanding benefits and costs in this symbiosis requires measuring how many prey bacteria are eaten, carried and left behind by infected hosts. We found thatParaburkholderiainfection makes hosts leave behind both symbionts and prey bacteria. However, the number of prey bacteria left uneaten was too small to explain why infected hosts produced fewer spores than uninfected hosts. Turning to carried bacteria, we found that hosts carry prey bacteria more often after developing in prey-poor environments than in prey-rich ones. This suggests that carriage is actively modified to ensure hosts have prey in the harshest conditions. Our results show that multi-faceted interactions with third parties shape the evolution of symbioses in complex ways.more » « less
-
A key question in cooperation is how to find the right partners and maintain cooperative relationships. This is especially challenging for horizontally transferred bacterial symbionts where relationships must be repeatedly established anew. In the social amoeba Dictyostelium discoideum farming symbiosis, two species of inedible Burkholderia bacteria (Burkholderia agricolaris and Burkholderia hayleyella) initiate stable associations with naive D. discoideum hosts and cause carriage of additional bacterial species. However, it is not clear how the association between D. discoideum and its carried Burkholderia is formed and maintained. Here, we look at precisely how Burkholderia finds its hosts. We found that both species of Burkholderia clones isolated from D. discoideum, but not other tested Burkholderia species, are attracted to D. discoideum supernatant, showing that the association is not simply the result of haphazard engulfment by the amoebas. The chemotactic responses are affected by both partners. We find evidence that B. hayleyella prefers D. discoideum clones that currently or previously carried Burkholderia, while B. agricolaris does not show this preference. However, we find no evidence of Burkholderia preference for their own host clone or for other hosts of their own species. We further investigate the chemical differences of D. discoideum supernatants that might explain the patterns shown above using a mass spectrometry based metabolomics approach. These results show that these bacterial symbionts are able to preferentially find and to some extent choose their unicellular partners. In addition, this study also suggests that bacteria can actively search for and target phagocytic cells, which may help us better understand how bacteria interact with immune systems.more » « less
An official website of the United States government

