Mosquito ingestion of antibodies against mosquito midgut microbiota improves conversion of ookinetes to oocysts for Plasmodium falciparum, but not P. yoelii

Bruce H. Noden, Jefferson A. Vaughan, Charles B. Pumpuni, John C Beier

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

The mosquito midgut is a site of complex interactions between the mosquito, the malaria parasite and the resident bacterial flora. In laboratory experiments, we observed significant enhancement of Plasmodium falciparum oocyst production when Anopheles gambiae (Diptera: Culicidae) mosquitoes were membrane-fed on infected blood containing gametocytes from in vitro cultures mixed with sera from rabbits immunized with A. gambiae midguts. To identify specific mechanisms, we evaluated whether the immune sera was interfering with the usual limiting activity of gram-negative bacteria in An. gambiae midguts. Enhancement of P. falciparum infection rates occurred at some stage between the ookinete and oocyst stage and was associated with greater numbers of oocysts in mosquitoes fed on immune sera. The same immune sera did not affect the sporogonic development of P. yoelii, a rodent malaria parasite. Not only did antibodies in the immune sera recognize several types of midgut-derived gram-negative bacteria (Pseudomonas spp. and Cedecea spp.), but gentamicin provided in the sugar meal 3. days before an infectious P. falciparum blood meal mixed with immune sera eliminated the enhancing effect. These results suggest that gram-negative bacteria, which normally impair P. falciparum development between the ookinete and oocyst stage, were altered by specific anti-bacterial antibodies produced by immunizing rabbits with non-antibiotic-treated midgut lysates. Because of the differences in developmental kinetics between human and rodent malaria species, the anti-bacterial antibodies had no effect on P. yoelii because their ookinetes leave the midgut much earlier than P. falciparum and so are not influenced as strongly by resident midgut bacteria. While this study highlights the complex interactions occurring between the parasite, mosquito, and midgut microbiota, the ultimate goal is to determine the influence of midgut microbiota on Plasmodium development in anopheline midguts in malaria endemic settings.

Original languageEnglish
Pages (from-to)440-446
Number of pages7
JournalParasitology International
Volume60
Issue number4
DOIs
StatePublished - Dec 1 2011

Fingerprint

Oocysts
Microbiota
Plasmodium falciparum
Culicidae
Eating
Malaria
Immune Sera
Anopheles gambiae
Antibodies
Bacterial Antibodies
Gram-Negative Bacteria
Parasites
Meals
Anti-Idiotypic Antibodies
Rodentia
Rabbits
Plasmodium
Pseudomonas
Gentamicins
Diptera

Keywords

  • Anopheles
  • Antibodies
  • Midgut microbiota
  • Plasmodium

ASJC Scopus subject areas

  • Parasitology
  • Infectious Diseases

Cite this

Mosquito ingestion of antibodies against mosquito midgut microbiota improves conversion of ookinetes to oocysts for Plasmodium falciparum, but not P. yoelii. / Noden, Bruce H.; Vaughan, Jefferson A.; Pumpuni, Charles B.; Beier, John C.

In: Parasitology International, Vol. 60, No. 4, 01.12.2011, p. 440-446.

Research output: Contribution to journalArticle

@article{5cd589e9cc2147c8aec65420a33f73e7,
title = "Mosquito ingestion of antibodies against mosquito midgut microbiota improves conversion of ookinetes to oocysts for Plasmodium falciparum, but not P. yoelii",
abstract = "The mosquito midgut is a site of complex interactions between the mosquito, the malaria parasite and the resident bacterial flora. In laboratory experiments, we observed significant enhancement of Plasmodium falciparum oocyst production when Anopheles gambiae (Diptera: Culicidae) mosquitoes were membrane-fed on infected blood containing gametocytes from in vitro cultures mixed with sera from rabbits immunized with A. gambiae midguts. To identify specific mechanisms, we evaluated whether the immune sera was interfering with the usual limiting activity of gram-negative bacteria in An. gambiae midguts. Enhancement of P. falciparum infection rates occurred at some stage between the ookinete and oocyst stage and was associated with greater numbers of oocysts in mosquitoes fed on immune sera. The same immune sera did not affect the sporogonic development of P. yoelii, a rodent malaria parasite. Not only did antibodies in the immune sera recognize several types of midgut-derived gram-negative bacteria (Pseudomonas spp. and Cedecea spp.), but gentamicin provided in the sugar meal 3. days before an infectious P. falciparum blood meal mixed with immune sera eliminated the enhancing effect. These results suggest that gram-negative bacteria, which normally impair P. falciparum development between the ookinete and oocyst stage, were altered by specific anti-bacterial antibodies produced by immunizing rabbits with non-antibiotic-treated midgut lysates. Because of the differences in developmental kinetics between human and rodent malaria species, the anti-bacterial antibodies had no effect on P. yoelii because their ookinetes leave the midgut much earlier than P. falciparum and so are not influenced as strongly by resident midgut bacteria. While this study highlights the complex interactions occurring between the parasite, mosquito, and midgut microbiota, the ultimate goal is to determine the influence of midgut microbiota on Plasmodium development in anopheline midguts in malaria endemic settings.",
keywords = "Anopheles, Antibodies, Midgut microbiota, Plasmodium",
author = "Noden, {Bruce H.} and Vaughan, {Jefferson A.} and Pumpuni, {Charles B.} and Beier, {John C}",
year = "2011",
month = "12",
day = "1",
doi = "10.1016/j.parint.2011.07.007",
language = "English",
volume = "60",
pages = "440--446",
journal = "Parasitology International",
issn = "1383-5769",
publisher = "Elsevier Ireland Ltd",
number = "4",

}

TY - JOUR

T1 - Mosquito ingestion of antibodies against mosquito midgut microbiota improves conversion of ookinetes to oocysts for Plasmodium falciparum, but not P. yoelii

AU - Noden, Bruce H.

AU - Vaughan, Jefferson A.

AU - Pumpuni, Charles B.

AU - Beier, John C

PY - 2011/12/1

Y1 - 2011/12/1

N2 - The mosquito midgut is a site of complex interactions between the mosquito, the malaria parasite and the resident bacterial flora. In laboratory experiments, we observed significant enhancement of Plasmodium falciparum oocyst production when Anopheles gambiae (Diptera: Culicidae) mosquitoes were membrane-fed on infected blood containing gametocytes from in vitro cultures mixed with sera from rabbits immunized with A. gambiae midguts. To identify specific mechanisms, we evaluated whether the immune sera was interfering with the usual limiting activity of gram-negative bacteria in An. gambiae midguts. Enhancement of P. falciparum infection rates occurred at some stage between the ookinete and oocyst stage and was associated with greater numbers of oocysts in mosquitoes fed on immune sera. The same immune sera did not affect the sporogonic development of P. yoelii, a rodent malaria parasite. Not only did antibodies in the immune sera recognize several types of midgut-derived gram-negative bacteria (Pseudomonas spp. and Cedecea spp.), but gentamicin provided in the sugar meal 3. days before an infectious P. falciparum blood meal mixed with immune sera eliminated the enhancing effect. These results suggest that gram-negative bacteria, which normally impair P. falciparum development between the ookinete and oocyst stage, were altered by specific anti-bacterial antibodies produced by immunizing rabbits with non-antibiotic-treated midgut lysates. Because of the differences in developmental kinetics between human and rodent malaria species, the anti-bacterial antibodies had no effect on P. yoelii because their ookinetes leave the midgut much earlier than P. falciparum and so are not influenced as strongly by resident midgut bacteria. While this study highlights the complex interactions occurring between the parasite, mosquito, and midgut microbiota, the ultimate goal is to determine the influence of midgut microbiota on Plasmodium development in anopheline midguts in malaria endemic settings.

AB - The mosquito midgut is a site of complex interactions between the mosquito, the malaria parasite and the resident bacterial flora. In laboratory experiments, we observed significant enhancement of Plasmodium falciparum oocyst production when Anopheles gambiae (Diptera: Culicidae) mosquitoes were membrane-fed on infected blood containing gametocytes from in vitro cultures mixed with sera from rabbits immunized with A. gambiae midguts. To identify specific mechanisms, we evaluated whether the immune sera was interfering with the usual limiting activity of gram-negative bacteria in An. gambiae midguts. Enhancement of P. falciparum infection rates occurred at some stage between the ookinete and oocyst stage and was associated with greater numbers of oocysts in mosquitoes fed on immune sera. The same immune sera did not affect the sporogonic development of P. yoelii, a rodent malaria parasite. Not only did antibodies in the immune sera recognize several types of midgut-derived gram-negative bacteria (Pseudomonas spp. and Cedecea spp.), but gentamicin provided in the sugar meal 3. days before an infectious P. falciparum blood meal mixed with immune sera eliminated the enhancing effect. These results suggest that gram-negative bacteria, which normally impair P. falciparum development between the ookinete and oocyst stage, were altered by specific anti-bacterial antibodies produced by immunizing rabbits with non-antibiotic-treated midgut lysates. Because of the differences in developmental kinetics between human and rodent malaria species, the anti-bacterial antibodies had no effect on P. yoelii because their ookinetes leave the midgut much earlier than P. falciparum and so are not influenced as strongly by resident midgut bacteria. While this study highlights the complex interactions occurring between the parasite, mosquito, and midgut microbiota, the ultimate goal is to determine the influence of midgut microbiota on Plasmodium development in anopheline midguts in malaria endemic settings.

KW - Anopheles

KW - Antibodies

KW - Midgut microbiota

KW - Plasmodium

UR - http://www.scopus.com/inward/record.url?scp=82155173546&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=82155173546&partnerID=8YFLogxK

U2 - 10.1016/j.parint.2011.07.007

DO - 10.1016/j.parint.2011.07.007

M3 - Article

C2 - 21763778

AN - SCOPUS:82155173546

VL - 60

SP - 440

EP - 446

JO - Parasitology International

JF - Parasitology International

SN - 1383-5769

IS - 4

ER -