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Nature| Wu Taihong et al. revealed the neural mechanism of pathogenic microorganisms to change host social behavior

 Last Update: 2023-02-03
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The invasion of pathogenic microorganisms or parasites can change the social behavior of the host animal, including mating, aggregation, invasion, communication, etc.
, which in turn affects the resistance and reproduction of individual animals, and ultimately affects the environmental adaptation and evolution
of species.
This phenomenon is prevalent in animals, such as: infection of pathogenic microorganisms in fruit flies prompts their dispersal; Baboons avoid mating with infected individuals of the opposite sex; Rabies virus alters the social behavior of animal or human hosts [1-4], but its neural mechanism needs to be studied in depth
.

Pseudomonas aeruginosa (P.
aeruginosa 14, PA14) is a gram-negative pathogenic bacterium that is widely distributed in nature and normal human skin, intestine and respiratory tract, and is one of
the more common conditional pathogenic bacteria in clinical practice.
The usual food for C.
elegans in the laboratory is E.
coli (E.
coli) OP50
.
When nematodes eat PA14 bacteria, PA14 accumulates in the intestine, causing damage to the host, increasing the expression of genes related to anti-pathogenic microorganisms, and killing nematodes
in about 3 days.

Pheromone is a small molecule released by animals, which is one of the
important factors that mediate social behavior.
The pheromones released by nematodes regulate a variety of behaviors
including mating, evasion, and aggregation.
Wu Taihong and other researchers reported in the 2019 Neuron article that pheromones inhibit the learning of PA14 bacteria by nematodes [5].

So the authors asked the question: Since pheromones inhibit the learning of PA14 bacteria by nematodes, does PA14 pretreatment change nematode perception of pheromones, thereby regulating their social behavior?
On January 4, 2023, Dr.
Wu Taihong and Dr.
Ge Minghai and other researchers from the team of Professor Yun Zhang's team from the Department of Evolutionary Biology and Center for Brain Science at Harvard University published a report entitled Pathogenic bacteria modulate pheromone in the journal Nature Response to Promote Mating's long study using Caenorhabditis elegans as a model animal reveals the neural mechanism
by which pathogenic microorganisms alter the social behavior of host nematodes.
By using behavioral methods, in vivo calcium imaging, single-cell transcriptome high-throughput sequencing (TRAP-RNA sequencing) and other research methods and techniques, the researchers found that the pretreatment of pathogenic microorganism PA14 induced the expression of GPCR receptor STR-44 in the food receptor AWA of adult hermaphroditic nematodes.
It gives AWA neurons a new function of pheromone reception, reduces the avoidance of pheromones by nematodes, and promotes their mating
with males.

Standard-cultured adult hermaphroditic nematodes dodge pheromones, and previous studies have shown that food sensory neurons AWA are not involved in pheromone perception
.
After 4-6 hours of conditioned treatment of adult hermaphroditic nematodes using PA14, the authors found that nematodes had a reduced or even tended to pheromone avoidance, and this process was mediated by direct pheromone perception by AWA neurons
.

Using single-neuron transcriptome high-throughput sequencing technology, the authors found that GPCR receptor STR-44 was induced to express
in AWA by PA14.
Using CRISPR-Cas9 technology, GFP knock-in nematode strains and str-44 gene deletion nematode strains were produced, and it was found that the expression of STR-44 as a pheromone receptor in AWA mediates pheromone feeling and reduces the avoidance
of pheromones by nematodes.
The transcription factor ZIP-5, histone H3K4 methylase SET-2, histone H3K27 demethylase JMJD-3.
1 and TRPV channel OCR-2 also regulate the expression of STR-44 in AWA and the dodging
of pheromones by nematodes.

a: Under standard culture conditions, food receptor neurons AWA did not participate in pheromone perception, and nematodes avoided pheromones to promote dispersion; b: After pretreatment with PA14, GPCR receptor STR-44 was induced to express in nematode AWA neurons, and AWA neurons could be directly activated
by pheromones.
The induced STR-44 in AWA inhibits nematode evasion of pheromones, reduces dispersion and promotes mating
.
The expression of pathogenic microorganism-induced str-44 is also regulated
by transcription factor ZIP-5, histone methylase SET-2, histone demethylase JMJD-3.
1 and TRPV channel OCR-2.

Finally, the authors elucidate the biological significance
of pathogenic bacteria-induced alteration of pheromone sensation.
Nematode hermaphrodites mainly reproduce through self-fertilization, but they still retain the ability to
mate with males.
Adult hermaphroditic nematodes cultured under standard conditions avoid pheromones, thereby reducing aggregation and promoting dispersion
.
The authors theorize that pretreatment of pathogenic bacteria will inhibit hermaphroditic nematode dodging pheromones and reduce dispersion, thereby promoting mating
with male nematodes.
To test this hypothesis, the authors designed experiments and found that the mating frequency of wild-type nematodes after PA14 pretreatment was significantly increased compared with the control group, and was mediated
by STR-44 in AWA.

In summary, this study reveals the causal mechanism by which pathogenic microorganisms induce the plasticity of social behavior in host animals, and this mechanism promotes genetic diversity and optimizes adaptability
to the environment.

In addition, the work was followed and reported by Nature Research Briefing.
https://doi.
org/10.
1038/d41586-022-04224-z (2023)）
。
Original link: https://doi.
org/10.
1038/s41586-022-05561-9

References

1.
Morran, L.
T.
, Schmidt, O.
G.
, Gelarden, I.
A.
, Parrish, R.
C.
, 2nd & Lively, C.
M.
Running with the Red Queen: host-parasite coevolution selects for biparental sex.
Science 333, 216-218, doi:10.
1126/science.
1206360 (2011).

2.
Keesey, I.
W.
et al.
Pathogenic bacteria enhance dispersal through alteration of Drosophila social communication.
Nat Commun8, 265, doi:10.
1038/s41467-017-00334-9 (2017).

3.
Paciencia, F.
M.
D.
et al.
Mating avoidance in female olive baboons (Papio anubis) infected by Treponema pallidum.
Sci Adv5, eaaw9724, doi:10.
1126/sciadv.
aaw9724 (2019).

4.
Hemachudha, T.
, Laothamatas, J.
& Rupprecht, C.
E.
Human rabies: a disease of complex neuropathogenetic mechanisms and diagnostic challenges.
Lancet Neurol1, 101-109, doi:10.
1016/s1474-4422(02)00041-8 (2002).

5.
Wu, T.
et al.
Pheromones modulate learning by regulating the balanced signals of two insulin-like peptides.
Neuron104, 1095-1109 e1095, doi:10.
1016/j.
neuron.
2019.
09.
006 (2019).

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