Diversity of Free-Living Environmental Bacteria and Their Interactions With a Bactivorous Amoeba

A small subset of bacteria in soil interact directly with eukaryotes. Which ones do so can reveal what is important to a eukaryote and how eukaryote defenses might be breached. Soil amoebae are simple eukaryotic organisms and as such could be particularly good for understanding how eukaryote microbi...

Full description

Bibliographic Details
Main Authors: Debra A. Brock, Tamara S. Haselkorn, Justine R. Garcia, Usman Bashir, Tracy E. Douglas, Jesse Galloway, Fisher Brodie, David C. Queller, Joan E. Strassmann
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-11-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fcimb.2018.00411/full
_version_ 1818259791151104000
author Debra A. Brock
Tamara S. Haselkorn
Justine R. Garcia
Usman Bashir
Tracy E. Douglas
Jesse Galloway
Fisher Brodie
David C. Queller
Joan E. Strassmann
author_facet Debra A. Brock
Tamara S. Haselkorn
Justine R. Garcia
Usman Bashir
Tracy E. Douglas
Jesse Galloway
Fisher Brodie
David C. Queller
Joan E. Strassmann
author_sort Debra A. Brock
collection DOAJ
description A small subset of bacteria in soil interact directly with eukaryotes. Which ones do so can reveal what is important to a eukaryote and how eukaryote defenses might be breached. Soil amoebae are simple eukaryotic organisms and as such could be particularly good for understanding how eukaryote microbiomes originate and are maintained. One such amoeba, Dictyostelium discoideum, has both permanent and temporary associations with bacteria. Here we focus on culturable bacterial associates in order to interrogate their relationship with D. discoideum. To do this, we isolated over 250 D. discoideum fruiting body samples from soil and deer feces at Mountain Lake Biological Station. In one-third of the wild D. discoideum we tested, one to six bacterial species were found per fruiting body sorus (spore mass) for a total of 174 bacterial isolates. The remaining two-thirds of D. discoideum fruiting body samples did not contain culturable bacteria, as is thought to be the norm. A majority (71.4%) of the unique bacterial haplotypes are in Proteobacteria. The rest are in either Actinobacteria, Bacteriodetes, or Firmicutes. The highest bacterial diversity was found in D. discoideum fruiting bodies originating from deer feces (27 OTUs), greater than either of those originating in shallow (11 OTUs) or in deep soil (4 OTUs). Rarefaction curves and the Chao1 estimator for species richness indicated the diversity in any substrate was not fully sampled, but for soil it came close. A majority of the D. discoideum-associated bacteria were edible by D. discoideum and supported its growth (75.2% for feces and 81.8% for soil habitats). However, we found several bacteria genera were able to evade phagocytosis and persist in D. discoideum cells through one or more social cycles. This study focuses not on the entire D. discoideum microbiome, but on the culturable subset of bacteria that have important eukaryote interactions as prey, symbionts, or pathogens. These eukaryote and bacteria interactions may provide fertile ground for investigations of bacteria using amoebas to gain an initial foothold in eukaryotes and of the origins of symbiosis and simple microbiomes.
first_indexed 2024-12-12T18:21:03Z
format Article
id doaj.art-b3494ba49d1e4b8a859ddb7ebbafacbd
institution Directory Open Access Journal
issn 2235-2988
language English
last_indexed 2024-12-12T18:21:03Z
publishDate 2018-11-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Cellular and Infection Microbiology
spelling doaj.art-b3494ba49d1e4b8a859ddb7ebbafacbd2022-12-22T00:16:08ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882018-11-01810.3389/fcimb.2018.00411417305Diversity of Free-Living Environmental Bacteria and Their Interactions With a Bactivorous AmoebaDebra A. Brock0Tamara S. Haselkorn1Justine R. Garcia2Usman Bashir3Tracy E. Douglas4Jesse Galloway5Fisher Brodie6David C. Queller7Joan E. Strassmann8Queller/Strassmann Laboratory, Washington University in St. Louis, Department of Biology, St. Louis, MO, United StatesQueller/Strassmann Laboratory, Washington University in St. Louis, Department of Biology, St. Louis, MO, United StatesQueller/Strassmann Laboratory, Washington University in St. Louis, Department of Biology, St. Louis, MO, United StatesQueller/Strassmann Laboratory, Washington University in St. Louis, Department of Biology, St. Louis, MO, United StatesQueller/Strassmann Laboratory, Washington University in St. Louis, Department of Biology, St. Louis, MO, United StatesMountain Lake Biological Laboratory, University of Virginia, Mountain Lake, VA, United StatesMountain Lake Biological Laboratory, University of Virginia, Mountain Lake, VA, United StatesQueller/Strassmann Laboratory, Washington University in St. Louis, Department of Biology, St. Louis, MO, United StatesQueller/Strassmann Laboratory, Washington University in St. Louis, Department of Biology, St. Louis, MO, United StatesA small subset of bacteria in soil interact directly with eukaryotes. Which ones do so can reveal what is important to a eukaryote and how eukaryote defenses might be breached. Soil amoebae are simple eukaryotic organisms and as such could be particularly good for understanding how eukaryote microbiomes originate and are maintained. One such amoeba, Dictyostelium discoideum, has both permanent and temporary associations with bacteria. Here we focus on culturable bacterial associates in order to interrogate their relationship with D. discoideum. To do this, we isolated over 250 D. discoideum fruiting body samples from soil and deer feces at Mountain Lake Biological Station. In one-third of the wild D. discoideum we tested, one to six bacterial species were found per fruiting body sorus (spore mass) for a total of 174 bacterial isolates. The remaining two-thirds of D. discoideum fruiting body samples did not contain culturable bacteria, as is thought to be the norm. A majority (71.4%) of the unique bacterial haplotypes are in Proteobacteria. The rest are in either Actinobacteria, Bacteriodetes, or Firmicutes. The highest bacterial diversity was found in D. discoideum fruiting bodies originating from deer feces (27 OTUs), greater than either of those originating in shallow (11 OTUs) or in deep soil (4 OTUs). Rarefaction curves and the Chao1 estimator for species richness indicated the diversity in any substrate was not fully sampled, but for soil it came close. A majority of the D. discoideum-associated bacteria were edible by D. discoideum and supported its growth (75.2% for feces and 81.8% for soil habitats). However, we found several bacteria genera were able to evade phagocytosis and persist in D. discoideum cells through one or more social cycles. This study focuses not on the entire D. discoideum microbiome, but on the culturable subset of bacteria that have important eukaryote interactions as prey, symbionts, or pathogens. These eukaryote and bacteria interactions may provide fertile ground for investigations of bacteria using amoebas to gain an initial foothold in eukaryotes and of the origins of symbiosis and simple microbiomes.https://www.frontiersin.org/article/10.3389/fcimb.2018.00411/fullDictyosteliumbacteriamicrobiomesymbiosisamoebaesociality
spellingShingle Debra A. Brock
Tamara S. Haselkorn
Justine R. Garcia
Usman Bashir
Tracy E. Douglas
Jesse Galloway
Fisher Brodie
David C. Queller
Joan E. Strassmann
Diversity of Free-Living Environmental Bacteria and Their Interactions With a Bactivorous Amoeba
Frontiers in Cellular and Infection Microbiology
Dictyostelium
bacteria
microbiome
symbiosis
amoebae
sociality
title Diversity of Free-Living Environmental Bacteria and Their Interactions With a Bactivorous Amoeba
title_full Diversity of Free-Living Environmental Bacteria and Their Interactions With a Bactivorous Amoeba
title_fullStr Diversity of Free-Living Environmental Bacteria and Their Interactions With a Bactivorous Amoeba
title_full_unstemmed Diversity of Free-Living Environmental Bacteria and Their Interactions With a Bactivorous Amoeba
title_short Diversity of Free-Living Environmental Bacteria and Their Interactions With a Bactivorous Amoeba
title_sort diversity of free living environmental bacteria and their interactions with a bactivorous amoeba
topic Dictyostelium
bacteria
microbiome
symbiosis
amoebae
sociality
url https://www.frontiersin.org/article/10.3389/fcimb.2018.00411/full
work_keys_str_mv AT debraabrock diversityoffreelivingenvironmentalbacteriaandtheirinteractionswithabactivorousamoeba
AT tamarashaselkorn diversityoffreelivingenvironmentalbacteriaandtheirinteractionswithabactivorousamoeba
AT justinergarcia diversityoffreelivingenvironmentalbacteriaandtheirinteractionswithabactivorousamoeba
AT usmanbashir diversityoffreelivingenvironmentalbacteriaandtheirinteractionswithabactivorousamoeba
AT tracyedouglas diversityoffreelivingenvironmentalbacteriaandtheirinteractionswithabactivorousamoeba
AT jessegalloway diversityoffreelivingenvironmentalbacteriaandtheirinteractionswithabactivorousamoeba
AT fisherbrodie diversityoffreelivingenvironmentalbacteriaandtheirinteractionswithabactivorousamoeba
AT davidcqueller diversityoffreelivingenvironmentalbacteriaandtheirinteractionswithabactivorousamoeba
AT joanestrassmann diversityoffreelivingenvironmentalbacteriaandtheirinteractionswithabactivorousamoeba