MOLECULAR AND ISOTOPIC SIGNATURES OF MICROORGANISMS IN LOW-OXYGEN MARINE ENVIRONMENTS

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MOLECULAR AND ISOTOPIC SIGNATURES OF MICROORGANISMS IN LOW-OXYGEN MARINE ENVIRONMENTS

Abstract

 

This dissertation explores the molecular and isotopic signatures of methanotrophic Archaea and the molecular signatures of cyanobacteria in low oxygen environments.  Archaeal ANerobic MEthaneotrophs (ANME) oxidize methane in anoxic sediment, and prevent methane, a potent greenhouse gas from reaching the atmosphere.  This process is hypothesized to take place via the reversal of methanogenesis based on culture and genetic evidence.  Coenzyme F430 is a tetrapyrrole used in the last step of methanogenesis, and likely enables the first step in reverse methanogenesis.  Therefore, the presence and concentration of F430 in association with AOM serves as a test for the reverse methanogenesis pathway in sediment.

In chapter 2, F430 was extracted, quantified, and isotopically analyzed in methanotrophic sediment from Hydrate Ridge and the Santa Monica Basin (west coast U.S.A).  The greatest amounts of F430 were recovered where sulfide, sulfate, and methane concentration profiles indicate the greatest AOM activity in the sediment.  These sediment horizons also contained the highest ANME-2 aggregate counts.  F430 was found to be isotopically distinct from methane and archaeal lipids, but similar to dissolved inorganic carbon (DIC). In the Hydrate Ridge and Santa Monica sediment F430 was ~60‰ enriched in 13C relative to archaeol lipids.

In chapter 3, the dual assimilation of methane and DIC is explored with a series of stable isotope labeling experiments using sediment from Hydrate Ridge and the Santa Monica Basin.  In experiments using Hydrate Ridge sediments, we observed the 13C label from DIC assimilated into archaeol, while in experiments using Santa Monica Basin sediment the 13C labeled from DIC and methane was assimilated into both F430 and lipids. The amount of DIC assimilated into F430 and lipids ranged from ~50% to 100%, with between 0% to 20% of carbon coming from methane.  Due to the amount of labeled methane that is oxidized to DIC we cannot be sure if methane is directly assimilated or first oxidized to DIC.  Coenzyme F430 was also only recovered from experiments where methane was added to the headspace, strengthening the link between F430 and methanotrophy.

Little Salt Springs is a sinkhole in Florida where a red biofilm in the euxinic water column produces large amounts of bacterialhopanetetrol (BHT), 2-methyl bacterialhopanetetrol (2-MeBHT) and 2-methyl anhydrobacterialhopanetetrol (2-MeAnhydroBHT).  The amount of each BHT produced varies seasonally and between years, with the geochemical cause of this variability unknown.  In chapter 4, a red cyanobacteria isolated from this biofilm was cultured under a number of different geochemical conditions in an attempt to identify possible causes for variability in bacteriohopanepolyols (BHP) production.  No single geochemical control was identified as amounts of BHT and 2-MeAnhydroBHT were similar in all experiments.  Future experiments should explore what effects oxygen concentration, fixed nitrogen species, trace metals, microbial community and combinations of different conditions have on BHP production.

 

 

 

 

Table of Contents 

 

List of Figures………………………………………………………………………………………………………………. vi

List of Tables……………………………………………………………………………………………………………… viii

Acknowledgements……………………………………………………………………………………………………….. x

Epigraph……………………………………………………………………………………………………………………… xi

Chapter 1: Introduction………………………………………………………………………………………………… 1

1.1. Anoxic methane oxidation…………………………………………………………………………………………. 1

1.2. ANME biochemistry………………………………………………………………………………………………… 2

1.3. Hopanoids……………………………………………………………………………………………………………… 4

1.4. Bacteriohopanepolyols……………………………………………………………………………………………… 4

1.5. Anticipated publications from this work………………………………………………………………………… 6

1.6. Figures and tables…………………………………………………………………………………………………….. 7

1.7. References……………………………………………………………………………………………………………. 14

Chapter 2: Carbon isotopic heterogeneity between ANME biomolecules………………………. 19

2.1. Abstract……………………………………………………………………………………………………………….. 19

2.2. Introduction………………………………………………………………………………………………………….. 19

2.3. Materials and Methods……………………………………………………………………………………………. 21

2.4. Results………………………………………………………………………………………………………………… 28

2.5. Discussion……………………………………………………………………………………………………………. 30

2.6. Conclusions………………………………………………………………………………………………………….. 33

2.7. Acknowledgements………………………………………………………………………………………………… 34

2.8. Figures and tables…………………………………………………………………………………………………… 34

2.9. References……………………………………………………………………………………………………………. 51

Chapter 3: Stable isotope probing of ANME carbon assimilation………………………………….. 55

3.1. Abstract……………………………………………………………………………………………………………….. 55

3.2. Introduction………………………………………………………………………………………………………….. 55

3.3. Methods………………………………………………………………………………………………………………. 57

3.4. Results………………………………………………………………………………………………………………… 66

3.5. Discussion……………………………………………………………………………………………………………. 68

3.6. Conclusions………………………………………………………………………………………………………….. 72

3.7. Acknowledgements………………………………………………………………………………………………… 72

3.8. Figures and tables…………………………………………………………………………………………………… 73

3.9. References……………………………………………………………………………………………………………. 93

Chapter 4: Quantifying Bacteriohopanepolyol production in Little Salt Springs cyanobacteria        96……………………………………………………………………………………………………………………………………….

4.1. Abstract……………………………………………………………………………………………………………….. 96

4.2. Introduction………………………………………………………………………………………………………….. 96

4.3. Methods………………………………………………………………………………………………………………. 98

4.4. Results………………………………………………………………………………………………………………. 101

4.5. Discussion………………………………………………………………………………………………………….. 102

4.6. Conclusions………………………………………………………………………………………………………… 104

4.7. Acknowledgements………………………………………………………………………………………………. 104

4.8. Figures and tables…………………………………………………………………………………………………. 105

4.9. References………………………………………………………………………………………………………….. 119

Chapter 5: Research summary…………………………………………………………………………………… 122

5.1. Chapter summaries……………………………………………………………………………………………….. 122

5.2. Future directions………………………………………………………………………………………………….. 123

5.3. References………………………………………………………………………………………………………….. 124

Appendix A: F430 abundance and isotope values from the Santa Monica basin…………… 126

A.1. Introduction……………………………………………………………………………………………………….. 126

A.2. Methods…………………………………………………………………………………………………………….. 126

A.3. Results………………………………………………………………………………………………………………. 130

A.4. Conclusions……………………………………………………………………………………………………….. 130

A.5. Figures and tables………………………………………………………………………………………………… 131

A.6. References…………………………………………………………………………………………………………. 132

Appendix B: Bacteriohopanepolyols through the Little Salt Springs water column……… 133

B.1. Introduction……………………………………………………………………………………………………….. 133

B.2. Methods…………………………………………………………………………………………………………….. 133

B.3. Results………………………………………………………………………………………………………………. 135

B.4. Conclusions……………………………………………………………………………………………………….. 135

B.5. Figures………………………………………………………………………………………………………………. 136

B.6. References…………………………………………………………………………………………………………. 137

Appendix C: F430 Extraction and Purification for quantification and Isotope analysis.. 138

C.1. Extraction………………………………………………………………………………………………………….. 138

C.2. Column chromatography……………………………………………………………………………………….. 139

C.3. HPLC Purification and quantification……………………………………………………………………….. 142

C.4. NANO-EA IRMS………………………………………………………………………………………………… 144

C.5. Figures and tables………………………………………………………………………………………………… 146

C.6. References…………………………………………………………………………………………………………. 149

Appendix D: Data tables……………………………………………………………………………………………. 150

Chapter 1: Introduction

 

 

1.1.          Anoxic methane oxidation

Methane, an important fuel for heating, transport and electricity generation, produces less carbon dioxide per energy yield than other fossil fuels (Marland et al., 2003).  Since the Kyoto protocol, governments have been exploring policies to encourage the use of natural gas over coal and oil (Apergis and Payne, 2010).  Growing demand has stimulated exploitation of unconventional natural gas sources such as methane clathrates, coalbed methane and methanogenic sediments (Administration, 2013, Collett, 2002)

Sedimentary basins along the coast of California and Oregon include numerous sites, among them Hydrate Ridge and the Santa Monica Basin, where natural gas could potentially be explored and produced.  In such regions, about half of sedimentary methane is prevented from reaching the atmosphere because it serves as an energy source for anaerobic oxidation of methane (AOM) by Archaea (Knittel and Boetius, 2009).  Methane oxidation in these sediments is linked to the reduction of sulfate, nitrate (Haroon et al., 2013), nitrite (Raghoebarsing et al., 2006), iron, or manganese (Beal et al., 2009).

AOM is commonly, but not exclusively, carried out by cell aggregates of Archaeal ANerobic

MEthanotrophs (ANME) and sulfate-reducing bacteria (SRB) (figure 1-1) (Boetius et al., 2000, Orphan et al., 2001b).  This syntrophic relationship was elegantly documented using fluorescent in situ hybridization with secondary ion mass spectrometry (FISH-SIMS) to trace both 13C and 15N incorporation in natural and enrichment studies into cell biomass (Orphan et al., 2001b, Orphan et al., 2009).  Working with natural isotope abundances, numerous studies have illustrated that methane is incorporated into biomass and the biochemical constituents of cells, most notably, membrane lipids (Table 1-1) (Hinrichs et al., 2000, House et al., 2009, Orphan et al., 2001a, Orphan et al., 2001b).

Methanotrophic Archaea comprise three broad phylogenetic lineages: ANME-1 ANME-2 and ANME-3 that are all distantly related to methanogens (Hallam et al., 2003, Lloyd et al., 2006, Orphan et al., 2002).  ANME-1 is distantly related to Methanosarcinales and Methanomicrobiales (Hinrichs et al., 1999), while ANME-2 and ANME-3 belong to the Methanosarcinales order (Hallam et al., 2003, Knittel et al., 2005, Lloyd et al., 2006, Orphan et al., 2001a) (figure 1-2).  All three groups have been identified and isotopically characterized in sediment from the

US western coast (Hydrate Ridge and the Eel River Basin) and Black Sea seeps (Boetius et al., 2000, Orphan et al., 2001b, Reitner et al., 2005, Treude et al., 2007).  Although isolation in pure culture for biochemical studies has proven difficult, ANME-1 from the Guaymas basin has been successfully enriched in culture (Holler et al., 2011).

ANME-1, 2 and 3 exhibit a number of distinct characteristics and occupy different ecological niches. ANME-1 cells are rectangular in shape and have been observed as single cells and in monospecific chains or clusters (Knittel et al., 2005, Lösekann et al., 2007, Orphan et al., 2002, Schubert et al., 2006).  They are loosely associated with sulfate-reducing bacteria but have been observed in microbial mats with layers of SRB (Knittel et al., 2005, Lösekann et al., 2007, Orphan et al., 2001a, Treude et al., 2007).  ANME-2 and 3 form spherical or shelllike cell aggregates comprised of an ANME core surrounded by SRB (Knittel et al., 2005, Lösekann et al., 2007, Orphan et al., 2002, Schubert et al., 2006, Treude et al., 2007).  ANME-1 tend to be more abundant in sulfatedepleted sediments (Yanagawa et al., 2011), hydrothermal environments (Dhillon et al., 2005, Kellermann et al., 2012) and environments with lower oxygen levels, as they are more sensitive to oxygen (Knittel et al., 2005).  In contrast, ANME-2 tend to be observed in shallow sediment depths and at higher sulfate concentration (Yanagawa et al., 2011).

 

1.2.         ANME biochemistry

A growing body of evidence indicates methanogenesis and methane oxidation take place simultaneously in marine sediments characterized by AOM.  Even so, field studies suggest the rate of methane oxidation outpaces methane generation by an order of magnitude or more, as shown by the co-occurrence of methane production and oxidation in Black Sea mats and in sediments from the Cascadia Margin (Treude et al., 2007, Yoshioka et al., 2010).

Bertram et al. (2013) recently demonstrated AMNE-1 and, especially, AMNE-2 in enrichment samples (from Black Sea sediments), can co-produce significant amounts of methane simultaneously with methane oxidation, at a production-to-oxidation ratio as high as 1:2.  This work also demonstrated that 13C-labeled carbon from C-1 substrates contributed carbon to biomass and membrane lipids (archaeol and hydroxyl-archaeol).   Bertram et al., (2013) revealed lipids in the AOM communities preferentially capture acetate and methanol carbon, when available, as well as carbon from bicarbonate.  This suggests ANME communities have significant metabolic flexibility, perhaps in response to H2 resources (Bertram et al., 2013), which potentially accounts for the extremely wide range of isotope signatures (~50 ‰) observed for AOM cell clusters in seep settings (House et al., 2009).

Anaerobic methanotrophy is hypothesized to proceed by the reversal of the methanogenesis pathway (Scheller et al., 2010, Zehnder and Brock, 1979).  This hypothesis, first proposed by Zehnder and Brock (1979), is supported by culture studies and genetic data (Hallam et al., 2004, Scheller et al., 2010).  Hallam et al., (2004) suggest that methane is oxidized to carbon dioxide and reduced by-products, with the assimilation of the reduced products. Alternatively, CO2 assimilation could proceed via the methanogenic pathway, with CO2 incorporated into methylene-tetrahydromethanopterin, which then enters the serine cycle, as in methanogenic Archaea (Angelaccio et al., 2003, Hallam et al., 2004, Taupp et al., 2010).  This reaction is catalyzed by serine hydroxymethyltransferase, an enzyme which so far has been reported in all sequenced archaeal genomes, including ANME (Angelaccio et al., 2003).

Culture studies of methanogenic Archaea that can carry out trace oxidation of methane provide supporting evidence for a reversed methanogenesis biochemical pathway.  The methanogen Methanosarcina acetovorines was shown to oxidize trace amounts of methane to CO2, as documented by observations that 13C-labeled methane became incorporated into CO2 (Moran et al., 2005).  Studies of Methanothermobacter marburgensis in pure culture demonstrated the last step in methanogenesis is also the first step in methane oxidation (Scheller et al., 2010).  This was documented by the incorporation of 13C-labeled methane into methyl-coenzyme M (2mercaptoethanesulfonate), which is used in the last step of methane production catalyzed by coenzyme F430 (figure 1-3).  Thus, if ANME oxidizes methane by reverse methanogenesis, F430 likely catalyzes the first step.

Genetic evidence from environmental samples provides additional support for reverse methanogenesis AOM.  Hallam et al. (2004) found genes that code for the enzymes used in methanogenesis, including for the last step, in ANME-1 and ANME-2 dominated samples from the Eel River Basin.  This suggests reverse methanogenesis capability is present among organisms in the sediment, and if the process takes place, signature coenzymes, such as F430, should also be present in the sediment.

Coenzyme F430 is a tetrapyrrole with a nickel center and was first identified by Gunsalus and Wolfe

(1978).  It is used in the last step of methanogenesis and is likely involved in the first step in the reverse pathway

(Hallam et al., 2004, Scheller et al., 2010).  Ten modified F430 coenzymes have been identified in methanogens and ANME dominated sediment(Allen et al., 2014, Mayr et al., 2008).  These modified F430 may be used in reactions other than methanogenesis and methanotrophy or are adaptations to environmental conditions (Allen et al., 2014). F430 is synthesized from glutamate, which is converted to 5-aminolevulinic acid via glutamyl-tRNA and glutamate1-semialdehyde (Friedmann and Thauer, 1986, Gilles et al., 1983, Pfaltz et al., 1987).  5-aminolevulinic acid is then converted to uroporphyrinogen III, the common precursor of tetrapyrroles (Gilles and Thauer, 1983, Pfaltz et al., 1987).  Unlike F430, ANME lipids that are synthesized from isoprenoids, are formed from acetyl-CoA via the mevalonate pathway (Goldstein and Brown, 1990, Smit and Mushegian, 2000).

Acetyl-CoA and glutamate could be formed from different sedimentary carbon sources, like dissolved inorganic carbon (DIC) and methane.  Potentially this could take place via a different part of the methanogenic pathway operating in different directions.  Methane is likely assimilated via a reversal of the last steps of reverse methanogenesis and converted to acetyl-CoA, while DIC may be assimilated via the first steps of methanogenesis, and converted to glutamate.  This means that F430 and lipids can be used to test the assimilation of DIC and methane in the sediment due to their synthesis from difference biological precursors.  F430 is, therefore, a target for reverse methanogenesis in the sediment and the assimilation of multiple carbon substrates

Chapters 2 and 3 aim to link coenzyme F430 in the sediment to AOM and ANME, something that has not been previously been established (Allen et al., 2014, Mayr et al., 2008).  In chapter 2, a link between AOM and F430 in Hydrate Ridge and Santa Monica Basin sediment is established from their concentration profiles.  Compound-specific isotope analysis of F430 and lipids reflect likely carbon sources in the sediment. The isotopic heterogeneity observed between lipids and F430 suggests ANME are biochemically flexible and able to assimilate methane carbon into their lipids and carbon from DIC into F430.

Chapter 3 evaluates underlying causes for the isotopic heterogeneity between ANME biomolecules identified in chapter 2 and explores implications for understanding isotopic variability that has been previously observed in House et al. (2009).  Stable isotope probing using 13C labeled methane and bicarbonate is used to explore the assimilation of carbon into F430 and lipids.  In Hydrate Ridge sediment, where ANME-1 is more abundant, DIC is shown to be assimilated into lipids with limited production of coenzyme F430.  In Santa Monica Basin sediment, where ANME-2 is more abundant, methane and DIC are both assimilated into F430 and lipids.

This work has been completed at the Pennsylvania State University under the supervision of Prof. Katherine H.

Freeman, in conjunction with Prof. Victoria J. Orphan and Dr. Katherine Dawson at the California Institute of Technology

 

1.3.        Hopanoids

Hopanoids (figure 1-4) are a class of pentacyclic compounds first identified in 1969 (Albrecht and Ourisson, 1969) and have been a useful tool in the study of ancient microbial life and the characterization of oil source rocks.  Because they are highly resistant to degradation, hopanoids are one of the most common geochemical compounds on the Earth (Ourisson and Albrecht, 1992).  Even though hopanoids are present throughout the rock record, the information they provide about the ancient microbial community is limited.  Interpretation about the types of ancient microbes are based on the position of a methyl group at the C2 (cyanobacteria) or C3

(methanotrophs and acetogenic bacteria) position (Cvejic et al., 2000, Farrimond et al., 2004, Rohmer et al., 1984, Summons et al., 1999).

2-Methyl hopanoids, found widely in Proterozoic sediments, are conventionally interpreted to represent the presence of ancient cyanobacteria (Summons and Walter, 1990, Summons et al., 1999).  This interpretation is based on the high proportion of 2-methyl bacteriohopanepolyols (BHPs) in cultured cyanobacteria and the belief that a cyanobacterial origin can account for the ubiquity of 2-methyl hopanoid across a range of environments and geological ages (Summons et al., 1999, Talbot et al., 2008).  Yet, this interpretation was challenged by genetic evidence that less than 10% of all modern bacteria are capable of producing BHPs and all currently known marine cyanobacteria don’t produce 2-methyl BHPs (Pearson et al., 2007, Talbot et al., 2008).

A greater understanding of the function and controls on 2-Methyl BHP production is needed to understand how well 2-Methyl hopanoids serve as a cyanobacteria marker.  Analytically this has proved challenging as different BHP structures can have vastly different detection response factors depending on the functional head group (figure 1-5), making quantification challenging.  Additionally, culturing studies exploring environmental effects on BHP production and distribution yield different lipid signatures in response to the same test parameters.  For example, experiments exploring the effects on N2 fixation using Frankia mycelia, Berry et al. (1993) observed and increase in BHP production, whereas Nalin et al. (2000) observed a decrease.

 

1.4.          Bacteriohopanepolyols

BHPs were first identified in 1973 (Förster et al., 1973) in bacteria, and are the biological precursor to geological hopanoids.  The BHP structure consists of a C30 triterpenoid pentacyclic hydrocarbon skeleton with a functional group attached at C22 (figure 1-6) (Talbot et al., 2003).  Sixty-three different functional groups have been identified so far.  Figure 1-7 illustrates most common forms in cyanobacteria cultures (Talbot et al., 2008).  When BHPs are preserved in the rock record, the reactive functional groups are lost, and as a result, interpretations about their sources in past environments are limited to the methyl position.

The function and distribution of BHPs through the bacterial domain is unclear (Fischer and Pearson, 2007).  Both gram negative and gram positive bacteria can produce BHPs, but not all bacteria contain the necessary squalene hopene cyclase gene for their production (Pearson and Rusch, 2009, Welander et al., 2010).  BHPs aren’t essential for life, even in bacteria that produce them, as demonstrated in knockout gene experiments using

Streptomyces and Rhodopseudomona (Seipke and Loria, 2009, Welander et al., 2010).  Initially, due to the structural similarity with sterols, it was suggested that they are used to regulate membrane permeability (Kannenberg and Poralla, 1999).  Numerous other studies have linked BHP production to membrane function and the physiological status of the bacterial cell (Jahnke et al., 1992, Jahnke et al., 1999, Joyeux et al., 2004, Ourisson et al., 1987, Poralla et al., 1980, Simonin et al., 1996).

BHPs have only been identified in culturable cyanobacteria, methanotrophs, acetic acid bacteria and anaerobic photosynthesizers.  While 41 species of cyanobacteria produce BHPs, only 19 of these are able to produce 2-methyl BHPs, the modern precursor of 2-methyl hopanoids, in pure culture (Pearson et al., 2007, Talbot et al.,

2008).  Further, 2-methyl BHPs have not been observed in modern marine sites with cyanobacteria (Pearson et al., 2007, Talbot et al., 2008).  This contradicts the interpretation of 2-methyl hopanoids in Proterozoic marine sediments that are believed to be from a cyanobacterial source.  Recently, a 2-methyl BHP producing cyanobacterium in the euxinic waters of a sinkhole, that is chemically analogous to the Proterozoic ocean, has been identified (Hamilton et al., Submitted).  Previously, cyanobacteria that produce 2-methyl BHP had only been found in hot springs (Jahnke et al., 2004) and terrestrial soils (Cooke et al., 2008).

The production of BHPs has been explored in a number of culture experiments using different oxygenic phototrophs.  BHP production has been shown to vary with a number of different parameters, including temperature, pH, nitrogen species and exposure to ethanol (Berry et al., 1993, Doughty et al., 2009, Poralla et al., 1980, Schmidt et al., 1986).  These experiments have yet to identify a reason why modern marine cyanobacteria don’t produce 2methyl BHPs.  Potentially this is due to the limited amount of studies that have quantified BHP structures.  Table 12 lists the studies that have quantified BHPs, with only Albrecht (2011), Doughty et al. (2009), and Welander et al. (2009) reporting changes in production in pure culture.  Only Albrecht (2011) has fully quantified individual BHP structures, allowing for different structures to be compared against each other.  Using the cyanobacteria isolated from Little Salt Springs and with accurate quantification, the geochemical controls on BHP production could be resolved.

The production of BHPs under different geochemical condition is explored using the Little Salt Springs cyanobacteria in chapter 4.  Similar amounts of bacteriohopanetetrol (BHT) and 2-methyl anhydro bacteriohopanetetrol (2-MeAnhydro BHT) were identified in the tested geochemical conditions and the control experiments. The recovered amount of BHT and 2-MeAnhydroBHT were lower than in biofilm samples, with 2methyl bacteriohopanetetrol and anhydrobacteriohopanetetrol identified in the biofilm not present in the culture experiments.  A clear geochemical control on production is not identified and future experiments should explore the effects of oxygen concentration, nitrogen species, trace metals and how combinations of different conditions affect BHP production. This work was completed at the Pennsylvania State University under the supervision of Prof. Katherine H. Freeman and Prof. Jennifer L. Macalady with culture samples supplied by Dr. Trinity Hamilton at the University of Cincinnati.

 

1.5.             Anticipated publications from this work

Chapter 2: Carbon Isotopic heterogeneity between ANME biomolecules, will be submitted to Environmental Microbiology with co-authors Jamey M. Fulton, Katherine S. Dawson Victoria J. Orphan and Katherine H. Freeman.

Chapter 3: Stable isotope probing of ANME carbon assimilation, will be submitted to Proceedings of the

National Academy of Science with co-authors, Katherine S. Dawson Victoria J. Orphan and Katherine H. Freeman

Chapter 4: Quantifying Bacteriohopanepolyol production in Little Salt Springs cyanobacteria, will be submitted to Organic Geochemistry with co-authors, Trinity Hamilton, Jennifer L. Macalady and Katherine H. Freeman

 

 

 

 

 

 

 

 

 

 

 

1.6.         Figures and tables

 

 

 

Figure 1-1: FISH image of ANME-2. This image was taken using sediment from the Santa Monica basin, which was used for a natural abundance study in chapter 2 and in incubation experiments using 13C substrates in chapter 3

 

 

Figure 1-2: ANME phylogenetic tree. 16S rRNA gene sequences tree from Knittel et al. (2005) showing how ANME-1, 2 and 3, in addition to their sub groups are related to each other.

 

Figure 1-3: Structure of co-enzyme F430. Ten additional F430 based structures have been identified in ANME and in methanogens and are believed to be used in functions other than methanogenesis (Allen et al., 2014).

 

 

 

 

Figure 1-4: Hopene. Also known as diploptene that has been observed in the rock record.

 

 

 

 

 

 

Figure 1-5: LCMS response to BHP structures. The response of 2-MeAnhydroBHT, BHT and pregenanediol used as a standard in the quantification of BHP compounds. Differences in the response of the two BHP compounds are due to the different polar head groups.

 

 

 

 

Figure 1-6: Red biofilm Bacteriohopanepolyols. These structure were identified in the cyanobacterial dominated biofilm from Little Salt Springs that is analyzed in chapter 4

 

Figure 1-7: BHP polar groups. Potential cyanobacterial BHP polar head groups as identified in Talbot et al.

(2008). Quantifying numerus BHP structures is difficult as these different polar groups produce different responses Table 1-1: ANME isotope values. Isotope values reported in previous studies of ANME at anoxic methanotrophic sites

                         Location                         Compound                δ 13C, ‰          Source                     Reference

Eel River Archaeol -104.1 ANME-2 (Orphan et al., 2001b)
Eel River Hydroxyarchaeol -107.6 ANME-2 (Orphan et al., 2001b)
Eel River Cell cluster -96 ANME-2 (Orphan et al., 2001b)
Eel River Archaeol -101.1 ANME-1/2 (Orphan et al., 2001a)
Eel River Archaeol -100.6 ANME-1/2 (Orphan et al., 2001a)
Eel River Archaeol -102.6 ANME-1/2 (Orphan et al., 2001a)
Eel River Archaeol -102.1 ANME-1/2 (Orphan et al., 2001a)
Eel River Hydroxyarchaeol -105.2 ANME-1/2 (Orphan et al., 2001a)
Eel River Hydroxyarchaeol -105.8 ANME-1/2 (Orphan et al., 2001a)
Eel River Hydroxyarchaeol -105.5 ANME-1/2 (Orphan et al., 2001a)
Eel River Hydroxyarchaeol -105.7 ANME-1/2 (Orphan et al., 2001a)
Eel River Archaeol -100 (Hinrichs et al., 2000)
Eel River hydroxyarchaeol -106 (Hinrichs et al., 2000)
Eel River Cells -24 to -87 ANME-1 (House et al., 2009)
Eel River Cells -18 to -75 ANME-2 (House et al., 2009)
Hydrate Ridge Archaeol -114 ANME-1 (Boetius et al., 2000)
Hydrate Ridge Hydroxyarchaeol -133 ANME-1 (Boetius et al., 2000)
Santa Barbra Basin Archaeol -119 (Hinrichs et al., 2000)
Santa Barbra Basin Hydroxyarchaeol -128 (Hinrichs et al., 2000)
Mediterranean mud volcanoes Archaeol -76.2 (Pancost et al., 2000)
Mediterranean mud volcanoes Archaeol -40.6 (Pancost et al., 2000)
Mediterranean mud volcanoes Archaeol -63.1 (Pancost et al., 2000)
Mediterranean mud volcanoes Archaeol -84.1 (Pancost et al., 2000)
Mediterranean mud volcanoes Archaeol -81.1 (Pancost et al., 2000)
Mediterranean mud volcanoes Archaeol -57.2 (Pancost et al., 2000)
Mediterranean mud volcanoes Archaeol -95.8 (Pancost et al., 2000)
Mediterranean mud volcanoes Archaeol -89 ANME-1 (Aloisi et al., 2002)
Mediterranean mud volcanoes Archaeol -97 ANME-1 (Aloisi et al., 2002)
Mediterranean mud volcanoes Hydroxyarchaeol -90 ANME-1 (Aloisi et al., 2002)
Mediterranean mud volcanoes Hydroxyarchaeol -97 ANME-1 (Aloisi et al., 2002)
Twentekanaal Netherlands Hydroxyarchaeol -67 ANME-2 (Raghoebarsing et al., 2006)
Black Sea Archaeol -95.6 ANME-1 (Reitner et al., 2005)
Black Sea Archaeol -87.9 (Michaelis et al., 2002)
Black Sea Hydroxyarchaeol -90 (Michaelis et al., 2002)
Black Sea Mat -66.4 ANME-1 (Treude et al., 2007)
Black Sea Mat -72.9 ANME-2 (Treude et al., 2007)

 

 

Table 1-2: BHT quantification. Other BHP structures are reported in these studies, but BHT is the only one present in all, allowing comparison between the studies.

Sample µg/g TLE BHP Quantification Reference
River 564 BHT Quantitative (Sáenz et al., 2011)
River 293 BHT Quantitative (Sáenz et al., 2011)
Estuary 318 BHT Quantitative (Sáenz et al., 2011)
Green Water 191 BHT Quantitative (Sáenz et al., 2011)
Blue water 81 BHT Quantitative (Sáenz et al., 2011)
Blue water 98 BHT Quantitative (Sáenz et al., 2011)
Pigeon creek sediment 25000 BHT Semi-quantitative (Pearson et al., 2009)
Grahams Harbour Sediment 30000 BHT Semi-quantitative (Pearson et al., 2009)
R. palustris Chemohetertrophic Exponential 3400 BHT Semi-quantitative (Welander et al., 2009)
R. palustris Chemohetertrophic

Stationary

3000 BHT Semi-quantitative (Welander et al., 2009)
R. palustris Photoheterotrophic Exponential 10000 BHT Semi-quantitative (Welander et al., 2009)
R. palustris Photoheterotrophic

Stationary

8000 BHT Semi-quantitative (Welander et al., 2009)
R. palustris pH5 2000 BHT Semi-quantitative (Welander et al., 2009)
R. palustris pH7 3000 BHT Semi-quantitative (Welander et al., 2009)
R. palustris pH9 2000 BHT Semi-quantitative (Welander et al., 2009)
L. ferrooxidans N source 692 BHT Quantitative (Albrecht, 2011)
L. ferrooxidans without N source 6934 BHT Quantitative (Albrecht, 2011)
L. ferrooxidans N source 3585 BHT Quantitative (Albrecht, 2011)
A.variablis photosynthetic 900 BHT Quantitative (Albrecht, 2011)
A.variablis photosynthetic 5500 BHT Quantitative (Albrecht, 2011)
A.variablis chemoheterotrophic 4 BHT Quantitative (Albrecht, 2011)
A.variablis chemoheterotrophic 400 BHT Quantitative (Albrecht, 2011)
Peat sample 10 BHT Quantitative (van Winden et al., 2012)
Peat sample 60 BHT Quantitative (van Winden et al., 2012)
N. punctiforme 500 BHT Semi-quantitative (Doughty et al., 2009)
N. punctiforme 2200 BHT Semi-quantitative (Doughty et al., 2009)
Microbial mat 6664 BHT Quantitative (Blumenberg et al., 2006)
Sediment 4920 BHT Quantitative (Blumenberg et al., 2006)
Sediment 2331 BHT Quantitative (Blumenberg et al., 2006)
Oxic zone 40 BHT Quantitative (Rush et al., 2014)
Transition zone 200 BHT Quantitative (Rush et al., 2014)
Transition zone 150 BHT Quantitative (Rush et al., 2014)
anoxic zone 600 BHT Quantitative (Rush et al., 2014)

anoxic zone                             100             BHT                 Quantitative                  (Rush et al., 2014)

 

 

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MOLECULAR AND ISOTOPIC SIGNATURES OF MICROORGANISMS IN LOW-OXYGEN MARINE ENVIRONMENTS

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