TY - JOUR
T1 - The functional significance of bacterial predators
AU - Hungate, Bruce A.
AU - Marks, Jane C.
AU - Power, Mary E.
AU - Schwartz, Egbert
AU - Groenigen, Kees Jan van
AU - Blazewicz, Steven J.
AU - Chuckran, Peter
AU - Dijkstra, Paul
AU - Finley, Brianna K.
AU - Firestone, Mary K.
AU - Foley, Megan
AU - Greenlon, Alex
AU - Hayer, Michaela
AU - Hofmockel, Kirsten S.
AU - Koch, Benjamin J.
AU - Mack, Michelle C.
AU - Mau, Rebecca L.
AU - Miller, Samantha N.
AU - Morrissey, Ember M.
AU - Propster, Jeffrey R.
AU - Purcell, Alicia M.
AU - Sieradzki, Ella
AU - Starr, Evan P.
AU - Stone, Bram W.G.
AU - Terrer, César
AU - Pett-Ridge, Jennifer
N1 - Funding Information:
This analysis was supported by the U.S. Department of Energy, Office of Biological and Environmental Research, Genomic Science Program (GSP) awards SCW1632 and DE-SC0020172 and by a Lawrence Fellow award to C.T. through the Lawrence Livermore National Laboratory. Studies surveyed in the meta-analysis were funded by DOE GSP awards DE-SC0016207, DE-SC0020172, SCW1024, and SCW1590 and by the U. S. National Science Foundation (DEB-1241094, DEB-1645596, DEB-1655357, and EAR-1124078). Work at LLNL was performed under the auspices of LLNL under contract DE-AC52-07NA27344.
Funding Information:
We appreciate the discussion from participants at the 2020 LLNL ?Microbes Persist? Soil Microbiome Scientific Focus Area meeting, which inspired this study. This analysis was supported by the U.S. Department of Energy, Office of Biological and Environmental Research, Genomic Science Program (GSP) awards SCW1632 and DE-SC0020172 and by a Lawrence Fellow award to C.T. through the Lawrence Livermore National Laboratory. Studies surveyed in the meta-analysis were funded by DOE GSP awards DE-SC0016207, DE-SC0020172, SCW1024, and SCW1590 and by the U. S. National Science Foundation (DEB-1241094, DEB-1645596, DEB-1655357, and EAR1124078). Work at LLNL was performed under the auspices of LLNL under contract DEAC52-07NA27344.
Publisher Copyright:
© 2021 Hungate et al.
PY - 2021
Y1 - 2021
N2 - Predation structures food webs, influences energy flow, and alters rates and pathways of nutrient cycling through ecosystems, effects that are well documented for macroscopic predators. In the microbial world, predatory bacteria are common, yet little is known about their rates of growth and roles in energy flows through microbial food webs, in part because these are difficult to quantify. Here, we show that growth and carbon uptake were higher in predatory bacteria compared to nonpredatory bacteria, a finding across 15 sites, synthesizing 82 experiments and over 100,000 taxon-specific measurements of element flow into newly synthesized bacterial DNA. Obligate predatory bacteria grew 36% faster and assimilated carbon at rates 211% higher than nonpredatory bacteria. These differences were less pronounced for facultative predators (6% higher growth rates, 17% higher carbon assimilation rates), though high growth and carbon assimilation rates were observed for some facultative predators, such as members of the genera Lysobacter and Cytophaga, both capable of gliding motility and wolf-pack hunting behavior. Added carbon substrates disproportionately stimulated growth of obligate predators, with responses 63% higher than those of nonpredators for the Bdellovibrionales and 81% higher for the Vampirovibrionales, whereas responses of facultative predators to substrate addition were no different from those of nonpredators. This finding supports the ecological theory that higher productivity increases predator control of lower trophic levels. These findings also indicate that the functional significance of bacterial predators increases with energy flow and that predatory bacteria influence element flow through microbial food webs. IMPORTANCE The word “predator” may conjure images of leopards killing and eating impala on the African savannah or of great white sharks attacking elephant seals off the coast of California. But microorganisms are also predators, including bacteria that kill and eat other bacteria. While predatory bacteria have been found in many environments, it has been challenging to document their importance in nature. This study quantified the growth of predatory and nonpredatory bacteria in soils (and one stream) by tracking isotopically labeled substrates into newly synthesized DNA. Predatory bacteria were more active than nonpredators, and obligate predators, such as Bdellovibrionales and Vampirovibrionales, increased in growth rate in response to added substrates at the base of the food chain, strong evidence of trophic control. This work provides quantitative measures of predator activity and suggests that predatory bacteria—along with protists, nematodes, and phages—are active and important in microbial food webs.
AB - Predation structures food webs, influences energy flow, and alters rates and pathways of nutrient cycling through ecosystems, effects that are well documented for macroscopic predators. In the microbial world, predatory bacteria are common, yet little is known about their rates of growth and roles in energy flows through microbial food webs, in part because these are difficult to quantify. Here, we show that growth and carbon uptake were higher in predatory bacteria compared to nonpredatory bacteria, a finding across 15 sites, synthesizing 82 experiments and over 100,000 taxon-specific measurements of element flow into newly synthesized bacterial DNA. Obligate predatory bacteria grew 36% faster and assimilated carbon at rates 211% higher than nonpredatory bacteria. These differences were less pronounced for facultative predators (6% higher growth rates, 17% higher carbon assimilation rates), though high growth and carbon assimilation rates were observed for some facultative predators, such as members of the genera Lysobacter and Cytophaga, both capable of gliding motility and wolf-pack hunting behavior. Added carbon substrates disproportionately stimulated growth of obligate predators, with responses 63% higher than those of nonpredators for the Bdellovibrionales and 81% higher for the Vampirovibrionales, whereas responses of facultative predators to substrate addition were no different from those of nonpredators. This finding supports the ecological theory that higher productivity increases predator control of lower trophic levels. These findings also indicate that the functional significance of bacterial predators increases with energy flow and that predatory bacteria influence element flow through microbial food webs. IMPORTANCE The word “predator” may conjure images of leopards killing and eating impala on the African savannah or of great white sharks attacking elephant seals off the coast of California. But microorganisms are also predators, including bacteria that kill and eat other bacteria. While predatory bacteria have been found in many environments, it has been challenging to document their importance in nature. This study quantified the growth of predatory and nonpredatory bacteria in soils (and one stream) by tracking isotopically labeled substrates into newly synthesized DNA. Predatory bacteria were more active than nonpredators, and obligate predators, such as Bdellovibrionales and Vampirovibrionales, increased in growth rate in response to added substrates at the base of the food chain, strong evidence of trophic control. This work provides quantitative measures of predator activity and suggests that predatory bacteria—along with protists, nematodes, and phages—are active and important in microbial food webs.
KW - Bdellovibrio
KW - Food webs
KW - O-HO
KW - Predator
KW - QSIP
KW - Stable isotope probing
KW - Top-down control
KW - Trophic interactions
UR - http://www.scopus.com/inward/record.url?scp=85104829872&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85104829872&partnerID=8YFLogxK
U2 - 10.1128/mBio.00466-21
DO - 10.1128/mBio.00466-21
M3 - Article
C2 - 33906922
AN - SCOPUS:85104829872
SN - 2161-2129
VL - 12
JO - mBio
JF - mBio
IS - 2
M1 - e00466-21
ER -