Bacterial metabolism of dissolved organic matter
Linking microbial ecolog y to ecosystem process from mountain to reef to ocean
Photo: Moorea Coral Reef LTER
Craig Nelson, Assistant Researcher Center for Microbial Oceanography: Research and Education (C-MORE)
Dept of Oceanography and UH Sea Grant University of Hawai‘i at Mānoa
Who I am, What I do, Where I’m going
• My areas of expertise and interest – Microbial community Metagenomics & Phylogenetics – Microbial biogeochemistry of Dissolved Organic Matter
• A few past projects and papers
– Alpine watershed microbial ecology/biogeochemistry – Coral reef biogeochemistry and microbial ecology
• A sampling of recent proposals • Projects I hope to pursue
Microbial Diversity: The Alien World
Microbial Diversity dwarfs all of the known diversity of plants and animals…
• Most bacterial phyla are uncultured and known only from gene fragments sequenced from the environment
Rappé and Giovannoni, Ann. Rev. Micro. 2003
Just the Bacteria
Microbial Diversity: The Alien World
Bacteria Regulate Ecosystems Ba
cter
ial B
iom
ass
Phytoplankton Biomass
Simon, et al. 1992 Mar. Ecol. Prog. Ser.
Unproductive systems are dominated by bacterial biomass
Earth’s Carbon Pools: Atmospheric CO2 = Terrestrial Plant Carbon = Aquatic Dissolved Organic Carbon “Dissolved organic carbon is almost exclusively accessible to heterotrophic bacteria” - Azam and Malfatti, Nature Reviews Microbiology 2007
– In almost any ecosystem, bacteria are responsible for a large fraction of aerobic respiration, all of the anaerobic respiration, and a large portion of the remineralization of organic nutrients.
• Cole, Ecosystems, 1999
What is a Metagenome? Whole community genomes from ~50 L of water Two Sizes of particles captured: 0.2um (free-living) and 5.0um (particle-attached) >600,000 DNA sequences each (~400 bp/read); matched against databases
DNA amplicon/shotgun pyrosequencing Bacterial/Archaeal phylogenetics and metagenomics
Analytical chemistry Fluorescence spectroscopy
Ecosystem metabolism Microbial community energetics
Bacterioplankton and Dissolved Organic Matter: Linking microbes to ecosystems
Complex dissolved organic matter pools
Diverse microbial communities
Dynamic ecosystem processes
Bacterioplankton and Dissolved Organic Matter: Linking microbes to ecosystems
Complex dissolved organic matter pools
Diverse microbial communities
Dynamic ecosystem processes
Landscape cover and resource exports
Habitat heterogeneity and algal/coral
exudates
Ecosystem Metabolism and Climate
Patterns
Phase shifts to algal
dominance
Alpine Lakes Sierra Nevada
Coral Reefs Moorea/Tahiti
Landscape microbial ecology
Land Cover
Climate
Resource Quality/Quantity
Microbial Community Structure & Metabolism
Ecosystem Process and Trophic Structure
a Human
Management
Case Study: Alpine Lakes of the Sierra Nevada, California
Image courtesy USGS GAP land cover database
Linking climate and landscape process with
resource delivery to downstream ecosystems
11,666 bodies of water above 2300 m >3000 larger than a typical “pond” (> 0.5 ha) Low Nutrient, Unproductive Ecosystems Are bacteria the dominant plankton? Who are they? What do they eat? What is their role in the ecosystem?
Sierra Nevada Lakes
GIS analysis by Steve Sadro, UCSB unpublished
Emerald Lake, 2800m
Land Cover
Climate
Resource Quality/Quantity
Microbial Community Structure & Metabolism
Ecosystem Process and Trophic Structure
a
Land Cover
Climate
Resource Quality/Quantity
Microbial Community Structure & Metabolism
Ecosystem Process and Trophic Structure
a
Nelson, Sadro, Melack 2009 L&O and 2012 Ecosystems
Diss
olve
d O
rgan
ic
Fluo
resc
ence
(nm
-1)
Bact
erio
plan
kton
(1
04 cel
ls m
L-1)
DIN
:DO
N m
olar
Di
ssol
ved
Nitr
ogen
Rat
io
Catchment Vegetation Cover
Mixed heirarchical regression modeling
Steve Sadro
John Melack
Land Cover
Climate
Resource Quality/Quantity
Microbial Community Structure & Metabolism
Ecosystem Process and Trophic Structure
a
Annual community phenology pattern repeated 2004, 2005, 2006
2004 2005 2006 b.
ICE COVER
SNOWMELT ICE-OFF STRATIFIED OVERTURN
NMS Ordination
Axis 1 – 54% Variance Best Correlate (r = 0.81): Snowmelt Discharge Axis 2 – 23% Variance Best Correlate (r = 0.73): Thermal Stability/Stratification
Nelson 2008 ISME Journal
Together: 75% Discriminant
Stra
tific
atio
n Discharge
Land Cover
Climate
Resource Quality/Quantity
Microbial Community Structure & Metabolism
Ecosystem Process and Trophic Structure
a
Nelson 2008 ISME Journal, Sadro et al 2011 L&O
Day of Year
Dept
h (m
)
2005
2009
1 3 5 7 9 1 3 5 7 9
phytoplankton
DOM
Flu
ores
cenc
e In
dex
McK
nigh
t et a
l 200
1 L&
O
Day of Year
terrestrial
Autotrophic Heterotrophic
Microbial Succession (linked to snowmelt) Changing DOM Sources (snowmelt terrigenous inputs) Seasonal shifts in Ecosystem Metabolic Balance
ICE COVER
2004 2005 2006
Informing Sustainable Management of Coastal Ecosystems
Land Cover
Climate
Resource Quality/Quantity
Microbial Community Structure & Metabolism
Ecosystem Process and Trophic Structure
a Human
Management
Tourism, Development, Wastewater, Aquaculture, Fisheries, SWAC, OTEC, etc.
ICE COVER
2004 2005 2006
Mo’orea, French Polynesia Site of Coral Reef Long Term Ecological Research Program Five years of Spatial Surveying among Offshore, Forereef, Backreef and Bay Habitats
Depleted DOC overlying the Reef Depleted bacterioplankton densities overlying the Reef
Spatial biogeochemical connectivity in nearshore tropical reef habitats
Nelson, et al. 2011 ISME Journal
BIG WAVES SMALL WAVES
Bacterioplankton cells Dissolved Organic Carbon
Nitrate Phosphate
Hypothesis: Labile DOM derived from reef benthic producers facilitates remineralization of recalcitrant oceanic DOM
Leichter et al. 2013, Oceanography
Bacterioplankton in the water column of reefs are different than those in the surrounding ocean
Nelson, Alldredge, McCliment, Amaral-Zettler, and Carlson. 2011. ISME Journal. Leichter et al. 2013, Oceanography
Non-metric multidimensional scaling of ~40 bacterial community structure samples by 16S rRNA T-RFLP
Phase shifts to algal dominance in Coral Reefs
Overfishing Nutrient Pollution
Images courtesy J. Smith
Hypothesis: Algal dissolved organic matter (DOM) exudates foster bacterial growth and oxygen removal, selecting for copiotrophic organisms and potential pathogens
15-30% of production as DOM – rich in saccharides (labile)
Smith et al. 2006 Ecology Letters
Boundary Layer
Hypoxia
Rosenberg et al. 2007 Oceanography
Pathogen facilitation
Maintenance of algal dominance by microbially-mediated feedbacks?
Turbinaria Brown Macroalgae
Ochrophyta
Halimeda Green Macroalgae
Chlorophyte
Amansia Red Macroalgae
Rhodophyte
Porites Hermatypic Coral
Cnidaria
8h Daylight Incubation Harvest DOM Exudate Sterile-filter (0.2 μm)
Inoculate with reef water 48h Dark Incubation
Track DOC, Oxygen, Cells
Effects of coral and algal exudates on bacterial growth
and oxygen demand
Photos a-c sourced from AlgaeBase: Guiry, M.D. & Guiry, G.M. 2011. http://www.algaebase.org, National University of Ireland, Galway; photo d sourced from MCR-LTER at http://mcr.lternet.edu/education with respective copyrights: a) Eric Coppejans( [email protected]); b) John Huisman ([email protected]); c) Heroen Verbruggen ([email protected]); d) Matthew Meier , MCRLTER.
Haas, Nelson, Kelly, Carlson, Rohwer, Leichter, Wyatt, Smith. 2011. PLoS ONE
Chloroflexi_SAR202
Deltaproteobacteria_SAR324
Deferribacteres_SAR406
Actinobacteria_Acidimicrobiales
Alphaproteobacteria_Rhodospirillaceae
Alphaproteobacteria_SAR116
Alphaproteobacteria_SAR11
Cyanobacteria_Synechococcus
Gammaproteobacteria_Oleiphilaceae
Betaproteobacteria_Methylophilaceae
Planctomycetes_Planctomycetaceae
Planctomycetes_OM190
Deltaproteobacteria_Bacteriovoraceae
Alphaproteobacteria_Erythrobacteraceae
Alphaproteobacteria_Kordiimonadaceae
Alphaproteobacteria_Hyphomonadaceae
Alphaproteobacteria_Sneathiellaceae
Alphaproteobacteria_Rhodobacteraceae
Flavobacteria_Flavobacteriaceae
Flavobacteria_Cryomorphaceae
Gammaproteobacteria_OMG
Gammaproteobacteria_Alteromonadaceae
Gammaproteobacteria_Oceanospirillaceae
Gammaproteobacteria_Pseudoalteromonadaceae
Gammaproteobacteria_Vibrionaceae
0.4 0.3 0.2 0.1
Community difference
(Unifrac distance weighted by
OTUs)
Elevated in Ambient Waters
& Controls
Elevated in Coral
Exudates
Elevated in Algal
Exudates
Mostly cultured copiotrophs: Gammaproteobacteria & Flavobacteria
Mostly uncultured Alphaproteobacteria
Mostly uncultured open ocean clades
Effects of coral and algal exudates on bacterial community composition (16S rRNA pyrosequencing)
Nelson, Goldberg, Kelly, Haas, Smith, Rohwer, Carlson. 2013. ISME Journal
Bro
wn
M
acro
alga
e G
reen
M
acro
alga
e R
ed
Mac
roal
gae
Cor
al
Con
trol
(P
lank
ton)
Am
bien
t R
eef W
ater
Communities differ by exudate source
Some Recent Proposals • Microbial Source Tracking (State of California Water Resources Board):
– Assessment of Bacterial Water Quality in the Lahontan Region: A study to provide data on bacterial indicator concentrations and sources of bacteria in surface waters
• Aquaculture and Microbes (NSF Small Business STTR/SBIR):
– KRuMBS: The Kyphosid Ruminant Microbial Biodigestor of Seaweeds: The alimentary microbiome of an herbivorous reef fish as a transformer of algal feedstocks
• Reef Ecosystem Biodiversity (NOAA):
– CREBON: The US Pacific Demonstration Coral Reef Ecosystem Biodiversity Observation Network
• Coral Microbial Ecology (NSF Biological Oceanography):
– Coral Microbiome Resilience to Macroalgal Exudates and Thermal Stressors
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