TY - JOUR
T1 - Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin
AU - Jaffe, Alexander L.
AU - Bardot, Corinne
AU - Le Jeune, Anne Hélène
AU - Liu, Jett
AU - Colombet, Jonathan
AU - Perrière, Fanny
AU - Billard, Hermine
AU - Castelle, Cindy J.
AU - Lehours, Anne Catherine
AU - Banfield, Jillian F.
N1 - Funding Information:
Funding was provided by the Berkeley Fellowship to A.L.J. and Moore Foundation Grant 71785 to J.F.B. Sequencing was partially supported by the NIH S10 OD018174 Instrumentation Grant.
Funding Information:
We thank Yue Clare Lou, Spencer Diamond, Shufei Lei, Adair Borges, Marie Schoelmerich, Lin-Xing Chen, Alex Thomas, and Rohan Sachdeva for helpful discussions and informatic support. We also thank Guillaume Borrel and François Enault for their comments on the manuscript, and Lily Law, Christopher Lefevre, and Didier Jézéquel for their assistance with sampling logistics. We also thank the Innovative Genomics Institute at UC Berkeley, Y. Justin Choi, Shana McDevitt, and QB3 Genomics at UC Berkeley.
Publisher Copyright:
© 2023, The Author(s).
PY - 2023/1/25
Y1 - 2023/1/25
N2 - Background: Permanently stratified lakes contain diverse microbial communities that vary with depth and so serve as useful models for studying the relationships between microbial community structure and geochemistry. Recent work has shown that these lakes can also harbor numerous bacteria and archaea from novel lineages, including those from the Candidate Phyla Radiation (CPR). However, the extent to which geochemical stratification differentially impacts carbon metabolism and overall genetic potential in CPR bacteria compared to other organisms is not well defined. Results: Here, we determine the distribution of microbial lineages along an oxygen gradient in Lac Pavin, a deep, stratified lake in central France, and examine the influence of this gradient on their metabolism. Genome-based analyses revealed an enrichment of distinct C1 and CO2 fixation pathways in the oxic lake interface and anoxic zone/sediments, suggesting that oxygen likely plays a role in structuring metabolic strategies in non-CPR bacteria and archaea. Notably, we find that the oxidation of methane and its byproducts is largely spatially separated from methane production, which is mediated by diverse communities of sediment methanogens that vary on the centimeter scale. In contrast, we detected evidence for RuBisCO throughout the water column and sediments, including form II/III and form III-related enzymes encoded by CPR bacteria in the water column and DPANN archaea in the sediments. On the whole, though, CPR bacteria and phages did not show strong signals of gene content differentiation by depth, despite the fact that distinct species groups populate different lake and sediment compartments. Conclusions: Overall, our analyses suggest that environmental gradients in Lac Pavin select for capacities of CPR bacteria and phages to a lesser extent than for other bacteria and archaea. This may be due to the fact that selection in the former groups is indirect and depends primarily on host characteristics. [MediaObject not available: see fulltext.].
AB - Background: Permanently stratified lakes contain diverse microbial communities that vary with depth and so serve as useful models for studying the relationships between microbial community structure and geochemistry. Recent work has shown that these lakes can also harbor numerous bacteria and archaea from novel lineages, including those from the Candidate Phyla Radiation (CPR). However, the extent to which geochemical stratification differentially impacts carbon metabolism and overall genetic potential in CPR bacteria compared to other organisms is not well defined. Results: Here, we determine the distribution of microbial lineages along an oxygen gradient in Lac Pavin, a deep, stratified lake in central France, and examine the influence of this gradient on their metabolism. Genome-based analyses revealed an enrichment of distinct C1 and CO2 fixation pathways in the oxic lake interface and anoxic zone/sediments, suggesting that oxygen likely plays a role in structuring metabolic strategies in non-CPR bacteria and archaea. Notably, we find that the oxidation of methane and its byproducts is largely spatially separated from methane production, which is mediated by diverse communities of sediment methanogens that vary on the centimeter scale. In contrast, we detected evidence for RuBisCO throughout the water column and sediments, including form II/III and form III-related enzymes encoded by CPR bacteria in the water column and DPANN archaea in the sediments. On the whole, though, CPR bacteria and phages did not show strong signals of gene content differentiation by depth, despite the fact that distinct species groups populate different lake and sediment compartments. Conclusions: Overall, our analyses suggest that environmental gradients in Lac Pavin select for capacities of CPR bacteria and phages to a lesser extent than for other bacteria and archaea. This may be due to the fact that selection in the former groups is indirect and depends primarily on host characteristics. [MediaObject not available: see fulltext.].
KW - Bacteriophages
KW - C1 metabolism
KW - CPR bacteria
KW - Meromictic lake
KW - Methane cycle
KW - RuBisCO
UR - http://www.scopus.com/inward/record.url?scp=85146758577&partnerID=8YFLogxK
U2 - 10.1186/s40168-022-01416-7
DO - 10.1186/s40168-022-01416-7
M3 - Article
C2 - 36694212
AN - SCOPUS:85146758577
SN - 2049-2618
VL - 11
JO - Microbiome
JF - Microbiome
IS - 1
M1 - 14
ER -