What shapes the metabolic and phylogenetic structure of microbial communities in aquatic systems?

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Carol Gilbert
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1 What shapes the metabolic and phylogenetic structure of microbial communities in aquatic systems? What is a microbial food web and what is the ecological importance?

2 Marine Microbial Food Web Dynamics The Biological Pump

3 Marine food webs Lalli and Parsons 1993

4 The Great Plate Anomaly in situ abundances (epifluorescent microscopy) Traditional plate counts

5 A changing paradigm

7 The Microbial Loop

8 The Microbial Loop

9 Microbial vs. Classical Food Webs PO 4 3- NH 4 + NO 3 - Nutrient remineralization Phytoplankton Bacterioplankton Zooplankton Charismatic megafauna Carbon sink (DOM & CO 2 )

10 Microbial vs. Classical Food Webs PO 4 3- NH 4 + NO 3 - Phytoplankton DOM Bacterioplankton Zooplankton Ciliates HNFs Microbial loop Charismatic megafauna

11 Why investigate Microbial Food webs? Most of the biomass in the oceans is microbial (<200um size class) Most of the production and consumption is by microbes (single celled prokaryotes and eukaryotes) Microbial food webs support production of larger organisms (interacts with the classical food web) Most nutrient regeneration occurs within the microbial food web Marine microbes are important in the C, N, P and Si cycles. Marine microbes are important in sediment formation (siliceous and calcareous oozes, organic aggregates and deposits)

12 Microbial Food Webs in Marine Systems Who are the players? What do they do? Why do we care? *Intro to the Plankton

13 Size classifications and terminology Classification of planktonic organisms is generally based upon size rather than function (most methods involve filtration which distinguishes organisms based upon size rather than species). This can be problematic because in the plankton, trophic position is not always determined by size (size ratios between predator and prey are not constant).

14 Abundance of living organisms Organism and size Bacterioplankton (~1um) Typical abundance 10 5 to 10 7 per ml Nanoflagellates (1-10um) 10 2 to 10 4 per ml Protizoan plankton (20-50um) 10 to 10 2 per ml Phytoplankton (20-200um) 10 to 10 4 per ml Humans (2m) 6x10 6 in Washington State

15 Bacterioplankton in Aquatic Systems Found in all natural waters Non-pathogenic! Small ( 1µm) yet abundant (>10 6 cells ml -1 ) Comparable in biomass to phytoplankton Fundamental in nutrient & carbon cycling Drive water quality parameters (i.e. anoxia, nutrient availability) Extremely diverse 10 µm (DAPI stained slide of bacterioplankton from Chesapeake Bay)

16 *Intro to the Plankton

Grazing mortality in microbial communities Defense strategies

immune system-like cell surface interactions Grazing involves

17 Grazing mortality in microbial communities Defense strategies involve pre and post ingestional mechanisms Phagotrophy involves immune system-like cell surface interactions Grazing involves many steps at which resistance can and does occur. Matz & Kjelleberg 2005 Fig. 1. Mechanistic steps in protistan prey capture that will potentially vary due to prey selectivity (Montagnes et al. 2008)

18 What shapes the metabolic and phylogenetic structure of microbial communities in aquatic systems?

19 DOM Bacterioplankton carbon metabolism Source Source Quality Availability Temperature Bacterial production (BP) BCC BGE Bacterial carbon growth consumption efficiency (BGE) (BCC) Nutrient form Relative and absolute concentration N&P Phylogeny Single-cell activity - DNA content - ETS activity Bacterial respiration (BR) Sink

20 Cross-System Patterns in Microbial Communities Estuaries Open Ocean total bacterial abundance beta attached bacteria CF gamma TSS POM/DOM nutrients free-living bacteria alpha Archaea RESUSPENSION Productivity, Carbon Flux, Growth Efficiencies

21 What is Biogeography? Spatial distribution of plant species across the globe is well documented and driven by predominantly by day length, precipitation, and temperature Global Plant Biomes Image from

22 Microbial Biogeography 5cm 2m 1cm 500m 100m

23 Microbial Biogeography Do microbes exhibit biogeographic patterns? How does community composition change over space and time in natural systems? What environmental factors shape these patterns? Science (Nov 2005)

24 Why study estuaries? Marine and freshwater communities are distinct Factors driving microbial diversity change rapidly Evidence of biogeographic patterns exists Global oceans (Baldwin et al. 2005; Pommier et al. 2005) Lakes (Crump et al. 2007; Reche et al. 2005; Wu et al. 2006) Estuaries? (Crump et al. 2004; Kirchman et al. 2005; Stepanauskus et al. 2003; Kan et al. 2006)

25 Experimental Design 1) Conduct a high-resolution sampling transect along the salinity gradient

26 Experimental Design 1) Conduct a high-resolution sampling transect along the salinity gradient 2) Visit a diverse range of estuarine systems

27 Experimental Design 1) Conduct a high-resolution sampling transect along the salinity gradient 2) Visit a diverse range of estuarine systems 3) Use denaturing gradient gel electrophoresis (DGGE) as an index of community composition

Experimental Design 1) Conduct a high-resolution sampling transect along the salinity gradient 2) Visit a diverse range of estuarine systems 3) Use

28 Experimental Design 1) Conduct a high-resolution sampling transect along the salinity gradient 2) Visit a diverse range of estuarine systems 3) Use denaturing gradient gel electrophoresis (DGGE) as an index of community composition 4) Identify patterns in community composition along the estuarine gradient

29 R/V Sharp Site Locations Puget Sound & Snohomish River Columbia River R/V Barnes PIE-LTER Delaware Bay Chesapeake Bay R/V Wecoma Winyah Bay/North Inlet Gulf of Mexico & Atchafalaya River R/V Pelican

30 Plum Island Sound LTER (25 km) Site Locations with transect lengths Delaware Bay (250 km) Winyah Bay NERR (30 km) Chesapeake Bay (300 km)

31 Site Locations with transect lengths Atchafalaya River/Gulf of Mexico (150 km) Snohomish River/ Puget Sound (300 km)

gradient of denaturants Extract DNA Amplify

32 Natural bacterioplankton community Fingerprinting with DGGE Banding pattern represents DNA fingerprint of each community Gel electrophoresis across gradient of denaturants Extract DNA Amplify 16s rrna genes with bacterial primers Images courtesy of Byron Crump

33 Fingerprinting with DGGE Banding patterns differ among stations JDS1 PS1 SN07 SN06 S05 SN04 SN03 SN02 SN01 Changes occur in presence vs. absence as well as density of bands Thus, dominant phylotypes shift as one moves from marine to fresh endmembers MARINE FRESH

34 Quantifying banding patterns: Multidimensional Scaling (MDS) Convert band presence vs. absence to binary data (1=present, 0=absent)

35 Quantifying banding patterns: Multidimensional Scaling (MDS) Convert band presence vs. absence to binary data (1=present, 0=absent) Create a similarity matrix of all bands (Dice correlation) S d = 2a/(b+c)

36 Quantifying banding patterns: Multidimensional Scaling (MDS) Convert band presence vs. absence to binary data (1=present, 0=absent) Create a similarity matrix of all bands (Dice correlation) S d = 2a/(b+c) Similarity matrix identifies percent similarity among samples

37 Quantifying banding patterns: Multidimensional Scaling (MDS) Convert band presence vs. absence to binary data (1=present, 0=absent) Create a similarity matrix of all bands (Dice correlation) S d = 2a/(b+c) Similarity matrix identifies percent similarity among samples Similarities are then visualized in two dimensions using MDS

38 Snohomish River Transect There is an obvious shift in composition along the estuarine gradient. sound river Changes in composition reflect distinct systems as well as environmental gradients.

39 Snohomish River Transect Changes in composition are well correlated with salinity Pattern suggests conservative mixing and simple dispersal

40 Gulf of Mexico and Delaware Bay river gulf meso plume oligo shelf poly eury Atchafalaya River/GOM Delaware Bay

41 Hypotheses on Biogeographic Patterns limited mixing with marine waters dilution/dispersal (short residence time) retention in mid-estuary (long residence time) dilution (longer residence time)

42 Hypotheses on Biogeographic Patterns Atchafalaya Snohomish Winyah Delaware

43 Take home message Estuarine bacterioplankton exhibit biogeographic variability Estuary-specific patterns exist and are predictable Freshwater communities persist in the estuary Changes in community composition are driven primarily by dispersal, but Longer residence times may allow the development of unique estuarine specific communities. More on this when we read Crump et al

The effect of agricultural nutrient loading on estuarine bacterioplankton communities

The effect of agricultural nutrient loading on estuarine bacterioplankton communities Jude Apple Horn Point Laboratory University of Maryland Center for Environmental Science Cambridge, Maryland What is