Symbiont-Induced Phagosome Changes Rather than Extracellular Discrimination Contribute to the Formation of Social Amoeba Farming Symbiosis

Tian, Yuehui; Peng, Tao; He, Zhenzhen; Wang, Luting; Zhang, Xurui; He, Zhili; Shu, Longfei

doi:10.1128/spectrum.01727-21

Cited by 10 publications

(13 citation statements)

References 51 publications

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“…Manipulation of phagosomes could also play a role in determining the contents of fruiting bodies. Paraburkholderia symbionts increase the pH of phagosomes, presumably to prevent host digestion of symbionts (Tian et al ., 2022). Similar modification of lysosomes is used by pathogens to evade human immune cells during infection (Isberg et al ., 2009; Leseigneur et al ., 2020).…”

Section: Discussionmentioning

confidence: 99%

“…We expected this result given the role of Paraburkholderia in causing hosts to carry food bacteria (DiSalvo et al ., 2015) and leave behind bacteria (Brock et al ., 2016b; Scott et al ., 2022). Infection with Paraburkholderia likely interferes with host digestion through modification of phagosomes (Tian et al ., 2022). This indigestion hypothesis is supported by our finding that Paraburkholderia infection did not affect development time (Figure 2).…”

Section: Discussionmentioning

confidence: 99%

“…These symbionts are specialized for interacting with amoebae (Shu et al ., 2018a; b; Brock et al ., 2020). Symbionts move towards hosts (Shu et al ., 2018b) and make host phagosomes less acidic so that the symbionts are not digested (Tian et al .,2022). One species of symbiont, P. hayleyella ,appears to have led to host adaptation in response to the presence of symbionts (Shu et al ., 2018a).…”

Section: Introductionmentioning

confidence: 99%

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Complex third-party effects in theDictyostelium-Paraburkholderiasymbiosis: prey bacteria that are eaten, carried, or left behind

Scott

Queller

Strassmann

2022

Preprint

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Symbiotic interactions change depending on the abundance of third parties like predators, prey, or pathogens. Third-party interactions with food bacteria are central to the symbiosis betweenDictyostelium discoideumsocial amoeba hosts and inedibleParaburkholderiabacterial symbionts. Symbiosis withParaburkholderiaallows hostD. discoideumto carry food bacteria through the dispersal stage where host amoebae aggregate and develop into fruiting bodies that disperse spores. Carrying bacteria benefits hosts when food bacteria are scarce but harms hosts when food bacteria are plentiful. The nature of this cost is unknown, but hosts leave bacteria behind when they carry symbionts. If this left-behind bacteria includes uneaten food bacteria, infected hosts may lose potential growth. Thus, decisions about how many food bacteria to eat, to carry, and to leave behind are crucial for understanding both benefits and costs in this symbiosis. We investigated how many food bacteria are uneaten and carried in this symbiosis by measuring fluorescently labeled food bacteria after fruiting body development. We found thatParaburkholderiainfection makes hosts leave both symbionts and uneaten food bacteria but leaving food bacteria uneaten did not explain costs to hosts. Counts of food bacteria in fruiting bodies showed that hosts carry more food bacteria after developing in food-poor environments than in food-rich. This indicates that hosts, and possiblyParaburkholderiasymbionts, actively modify how many food bacteria are carried to ensure hosts have food in the harshest conditions. Decisions about how many third-party bacteria to eat, carry, or leave may thus have important effects on this symbiosis.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Complex third-party effects in theDictyostelium-Paraburkholderiasymbiosis: prey bacteria that are eaten, carried, or left behind

Scott

Queller

Strassmann

2022

Preprint

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“…This food carriage is mostly extracellular and varies by Paraburkholderia genotype and food bacterial species (Khojandi et al, 2019; Miller et al, 2020). Recent work has shown that Paraburkholderia symbionts inhibit phagosome acidification (Tian et al, 2022), suggesting that food carriage could be mediated by the creation of a more hospitable environment for other bacteria that get ingested. In the soil environment, however, many fruiting bodies contain microbiota, both with and without Paraburkholderia (Brock et al, 2018; Sallinger et al, 2021), and in our study, Paraburkholderia did not increase the diversity of this microbiota.…”

Section: Discussionmentioning

confidence: 99%

The complexities of inferring symbiont function: Paraburkholderia symbiont dynamics in social amoeba populations and their impacts on the amoeba microbiota

DuBose

Robeson

Hoogshagen

et al. 2021

Preprint

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The relationship between the social amoeba Dictyostelium discoideum and its endosymbiotic bacteria Paraburkholderia provides a model system for studying the development of symbiotic relationships. Laboratory experiments have shown that any of three species of Paraburkholderia symbiont allow D. discoideum food bacteria to persist through the amoeba lifecycle and survive in amoeba spores, rather than being fully digested. This phenomenon is termed "farming", as it potentially allows spores dispersed to food poor locations to grow their own. The occurrence and impact of farming in natural populations, however, has been a challenge to measure. Here, we surveyed natural D. discoideum populations and found that only one of the three symbiont species, P. agricolaris, remained prevalent. We then explored the effect of Paraburkholdia on the amoeba microbiome, expecting that by facilitating bacterial food carriage it would diversify the microbiome. Contrary to our expectations, Paraburkholderia tended to infectiously dominate the D. discoideum microbiome, in some cases decreasing diversity. Similarly, we found little evidence for Paraburkholderia facilitating the carriage of particular food bacteria. These findings change our understanding of farming and suggest the possibility that Paraburkholderia could be playing multiple roles for its host, as inferred metagenomic analysis indicates a potential role of P. agricolaris in toxin degradation.

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“…This study used a model amoeba Dictyostelium discoideum QS9 for all experiments (Tian et al, 2022; Zhang et al, 2022). D. discoideum was grown from previously frozen spores on SM/5 agar plates (2 g glucose, 2 g BactoPeptone (Oxoid), 2 g yeast extract (Oxoid), 0.2 g MgCl 2 , 1.9 g KH 2 PO 4 , 1 g K 2 HPO 4 , and 15 g agar per liter) with food bacterium Klebsiella pneumoniae (obtained from the Dicty Stock Center) at 21°C.…”

Section: Methodsmentioning

confidence: 99%

Environmental stress promotes the persistence of facultative bacterial symbionts in amoebae

Wang

Huang

Mai

et al. 2023

Ecology and Evolution

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Amoebae are single-celled protists that are widely found in water, soil, and other natural habitats (Samba-Louaka et al., 2019;Zheng et al., 2022). They have also been found in engineered systems such as swimming pools and drinking water systems (Delafont et al., 2013;Thomas et al., 2006;Thomas & Ashbolt, 2011). Amoebae are a significant threat to human health because some of them are pathogenic and even lethal to humans (Shi et al., 2021;Thomas & Ashbolt, 2011). In addition, diverse microbes, including bacteria, fungi, and viruses, many of which are human pathogens, have been found hidden within amoebae (Shi et al., 2021;Strassmann & Shu, 2017). For example, Legionella pneumophila can reside within amoebae, using them as their replication hosts (Hoffmann et al., 2014). Moreover, recent studies suggest that amoebae are resistant to drinking water disinfection and further protect their intracellular bacteria from disinfection (He et al., 2021(He et al., , 2022. Therefore, both amoebae and their bacterial symbionts are a significant threat to public health, and a better understanding of their interactions is in urgent need.

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Symbiont-Induced Phagosome Changes Rather than Extracellular Discrimination Contribute to the Formation of Social Amoeba Farming Symbiosis

Abstract: Protists are single-celled, extremely diverse eukaryotic microbes. Like animals and plants, they live with bacterial symbionts and have complex relationships.

Cited by 10 publications

References 51 publications

Complex third-party effects in theDictyostelium-Paraburkholderiasymbiosis: prey bacteria that are eaten, carried, or left behind

Complex third-party effects in theDictyostelium-Paraburkholderiasymbiosis: prey bacteria that are eaten, carried, or left behind

The complexities of inferring symbiont function: Paraburkholderia symbiont dynamics in social amoeba populations and their impacts on the amoeba microbiota

Environmental stress promotes the persistence of facultative bacterial symbionts in amoebae

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