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7 Cross-Feeding and Competition in Anaerobic Dehalogenating Microbial Communities

7 Cross-Feeding and Competition in Anaerobic Dehalogenating Microbial Communities

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in anaerobic dehalogenating microbial communities when the appropriate electron

acceptor is available. The effect of competition on OHRB and their dehalogenation performance may result from competition between different species of OHRB

for the same halogenated electron acceptor, or from competition between OHRB

and other anaerobic bacteria for electron donor due to the presence of alternative

electron acceptors, such as sulfate, nitrate, iron, and others.

Anaerobic dehalogenating microbial communities grown on different halogenated compound classes typically comprise obligate and facultative OHRB growing

together in stable enrichment cultures. Combinations include Desulfitobacterium

and Dehalococcoides (Rouzeau-Szynalski et al. 2011; Ise et al. 2011; Yang

et al. 2005), Dehalococcoides and Dehalobacter (Grostern and Edwards 2006b;

Daprato et al. 2007), Dehalococcoides and Geobacter (Duhamel et al. 2002;

Ziv-El et al. 2012; Ritalahti et al. 2006), Sulfurospirillum and Dehalococcoides

(Maillard et al. 2011; He et al. 2006), and often more than two genera:

Dehalococcoides, Desulfuromonas, Desulfitobacterium (Ballerstedt et al. 2004),

Dehalogenimonas, Dehalobacter and Dehalococcoides (Manchester et al. 2012),

and Dehalococcoides, Dehalobacter and Desulfitobacterium (Vandermeeren et al.

2014). Even when only a single OHRB genus is present, multiple distinct strains

are often observed. This has been shown in cultures dechlorinating chloroalkenes/

alkanes (Duhamel et al. 2002; Duhamel and Edwards 2006; Daprato et al. 2007;

Futagami et al. 2011; Ritalahti et al. 2006; Brisson et al. 2012; Vainberg et al.

2009; Tang and Edwards 2013), chlorobenzenes (Nelson et al. 2011, 2014) and

PCBs (Watts et al. 2001; Fagervold et al. 2005).

Certain Monod kinetic-based models have explored competition between different OHRB genera (Becker 2006; Becker and Seagren 2009; Lai and Becker

2013). For example, Becker and Seagren (2009) modeled competition between

Dehalococcoides and Desulfuromonas michiganensis and the implications for

PCE DNAPL bioenhancement. They concluded that the potential for bioenhancement of DNAPL was better at low flow velocity. Chen et al. (2013) also explored

and modeled enhanced DNAPL dissolution in a column setting. Geobacter and

Dehalococcoides were the modeled populations. Enhanced dissolution showed

high sensitivity to Dehalococcoides kinetic constants for PCE and cDCE as

well as Dehalococcoides growth. In a dual Monod model for Dehalobacter and

Dehalococcoides grown on PCE in coculture with non-limiting H2 levels, Lai and

Becker (2013) conclude that accurate models required that both competition and

inhibition should be considered.

When multiple electron acceptors are simultaneously present, OHRB will

complete with other anaerobic respiring bacteria for resources, primarily electron donor, and the availability of electron donor generally governs the order of

terminal electron acceptor utilization. When electron donor is limiting, the most

energy-yielding electron-accepting processes and associated organisms will be

favored thermodynamically (Fennell and Gossett 1998; Smatlak et al. 1996).

When electron donor is in excess, multiple electron-accepting processes will occur

simultaneously. In most laboratory enrichment cultures, the only external electron acceptor added is the organohalide of interest though CO2 as bicarbonate is



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typically present in the medium, and donor is often in excess, thus methanogenesis, acetogenesis, and dechlorination occur simultaneously. Then, when alternate terminal electron acceptors are added, the microbial community tends to

change significantly. Iron reducers, sulfate reducers, and even denitrifiers have

been reported in OHRB communities when the appropriate electron acceptor is

added. Wei and Finneran (2013) reported methanogenesis, iron reduction, and sulfate reduction are simultaneous with OHRB. Higher acetate levels did not speed

up reductive dechlorination but instead increased methanogenesis. In membrane

bioreactors TCE, 1,1,1-TCA, and CF were reductively dehalogenated even in the

presence of nitrate and sulfate reduction (Zhang et al. 2010). Aulenta et al. (2007)

maintained cultures on a variety of electron donors with concurrent reduction of a

mixture of electron acceptors [chlorinated ethenes, nitrate, sulfate, and Fe(III)] but

they reported that over 99 % of the reducing equivalents were channeled to alternate electron acceptors rather than organohalides. In others reports, the generated

sulfide and/or the competition with sulfate reducers for electron donors diminished

reductive dechlorination when sulfate was provided. For example, parallel PCEdechlorinating chemostats were established and sulfate was fed to one (at 1 mM)

(Berggren et al. 2013). Reductive dechlorination efficiency decreased following

the onset of complete sulfate reduction—with VC and cDCE rather than ethene as

the major end product. In the trichlorobenzene-dechlorinating enrichment culture

that ultimately yielded Dehalococcoides strain CBDB1, sulfate addition clearly

inhibited reductive dechlorination (Adrian et al. 1998). The ecological principles

of competition for resources are equally applicable in OHRB communities. In the

typically resource limited natural environments, thermodynamic thresholds for

growth are critical, and in this context OHRB do well, because the energy from

dehalogenation is typically greater than that from methanogenesis, acetogenesis, or sulfate reduction, but growth is generally limited by low concentrations

of electron acceptor. In artificial situations of contaminated sites or bioreactors,

conditions can be tailored or created to channel electrons from available donors to

dehalogenation. Much effort has been focused on the value of different donors in

this regard, owing to these donors being the driver of cost for remediation. Models

that consider the whole microbial community often incorporate thermodynamic

thresholds for competing electron-accepting processes, as reviewed in (Häggblom

and Bossert 2003; Chambon et al. 2013).



13.8 Summary

Inhibition and competition within OHRB communities are clearly a complex multilayered subject. Nevertheless, enzyme assays carried out with crude cell extracts

confirm that some halogenated compounds interact and inhibit certain reductive

dehalogenases in a quantifiable and reproducible manner, indicating that inhibition is often a direct result of a specific interaction with a dehalogenase protein



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complex. A systematic approach starting from known enzymes and cultures to

obtain meaningful data may preclude some of the frustrations among experimentalists and modelers alike in attempts to reconcile data to find adequate model

parameters for meaningful simulations. An on-going dialog between experimentalists and modelers is needed to obtain approximations that do not over simplify

dominant rate-limiting steps. Moreover, too many studies invoke inhibition without any consideration of the concentrations at which these effects are measured.

Fundamentally, the inhibition constants (Ki) reflect the affinity of inhibitors for

their target and provide the inhibitor concentration that causes substantial inhibition (typically 50 %) of the process. While the values of Ki differ depending on

the model type (e.g., competitive, noncompetitive, uncompetitive or Haldane

or other), in the context of field work and the errors associated with the many

assumptions and data that enter a model, they provide an adequate approximate

measure of relative potency and a place to begin, regardless of model. The many

Ki values reported in the literature for chlorinated solvents, many summarized in

recent publications (Lai and Becker 2013; Chambon et al. 2013) and others illustrated herein (Chan et al. 2011; Grostern et al. 2009; Wei 2012) provide useful

guidelines for practitioners to decide whether co-contaminant concentrations in a

particular situation are likely or not to affect the microbial reductive dechlorination of the target contaminants.

Inhibition constants, just like Km, Vmax, pH, T optima, co-factors, and substrate

ranges are intrinsic properties particular to each enzyme and reflect the underlying structural properties of the protein. These properties should be measured as

part of the data sets required for more complete protein characterization. As more

and more reductive dehalogenases are identified, purified, and characterized more

fully, patterns among these interactions will become more clear and more robust

inhibition constants or models of activity will be available, leading to increased

insight into the mechanism of the reactions catalyzed by these enzymes, as well as

to more practically useful models of dehalogenation.

Similarly, now that we can monitor complete microbial communities using

rapid and inexpensive sequencing tools, we are beginning to see more accurate

analysis of inhibition and competition effects in mixed communities, and better

modeling of microbial population dynamics and function. This window into the

community is opening ever-wider and revealing new levels of complexity but also

monitoring tools to track and predict governing patterns of resource allocation and

utilization. The analysis of microbiome function is not only being driven by environmental processes as in past decades, but now has received enormous attention

from human health biology and agriculture as well. The next decade of research

is bound to reveal remarkable dynamics within these communities that contribute

significantly to their function and evolution, and to the health of the planet and all

its inhabitants.

Acknowledgements  The authors acknowledge the contributions of the many students,

postdocs, and industrial and academic collaborators who have contributed to the research and

insights into reductive dehalogenation and anaerobic microbial processes over the years.



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Chapter 14



Organohalide-Respiring Bacteria

as Members of Microbial Communities:

Catabolic Food Webs and Biochemical

Interactions

Ruth E. Richardson

Abstract Organohalide-respiring bacteria (OHRB) have been isolated from a

wide range of anoxic environments worldwide and can easily be enriched in the

laboratory. Obligate OHRB generally thrive best in mixed communities as part

of anaerobic food webs that typically involve interspecies hydrogen (H2) transfer from fermenters to OHRB, and often OHRB compete for H2 with hydrogenotrophic methanogens. In laboratory enrichments, the community composition of

the non-OHRB fraction of the communities is dependent on which electron donor

is used for enrichment as well as other factors (e.g., the concentrations of organohalide substrate). In addition to catabolic food webs, other biochemical interactions in these communities include provision of key cofactors (e.g., corrinoids),

relief of toxicity due to reactive oxygen species, as well as the organohalides

themselves. Multiple OHRB often coexist stably in enrichment cultures and environmental communities. This diversity in OHRB populations creates complex

interactions among different OHRB—with the partially dehalogenated end product of one population serving as substrate for other populations. Recent broad

surveys of bacterial and archaeal community structure at sites undergoing in situ

bioremediation are confirming that fermenters, methanogens, and OHRB are all

stimulated by enhanced bioremediation efforts but that aerobes including methanotrophs and organohalide-oxidizing aerobes are also stimulated—especially

in downgradient plume regions. The chapter will also discuss roles of OHRB

populations in pristine environments including soils and sediments where they

dehalogenate naturally produced halogenated organic matter and may compete

with sulfate reducers and iron reducers when appropriate electron acceptors are

available.



R.E. Richardson (*) 

School of Civil and Environmental Engineering, Cornell University, Ithaca, NY, USA

e-mail: rer26@cornell.edu

© Springer-Verlag Berlin Heidelberg 2016

L. Adrian and F.E. Löffler (eds.), Organohalide-Respiring Bacteria,

DOI 10.1007/978-3-662-49875-0_14



309



310



R. Richardson



Abbreviations

Dhc

Dehalococcoides

OHRBOrganohalide-respiring bacteria

Dhb

Dehalobacter

RDaseReductive dehalogenase

PCETetrachloroethene

TCETrichloroethene

cis-DCE

cis-1,2-dichloroethene

VCVinyl chloride

DNAPLDense nonaqueous phase liquid

PCBsPolychlorinated biphenyls



14.1 Introduction

Enrichment cultures with organohalide-respiring capabilities have led to isolation

of various Organohalide-respiring bacteria (OHRB). Pure culture studies have enabled metabolic characterization of the OHRB including electron donor range characterization and range of organohalides used as electron acceptors. Though pure

culture work is essential for such fundamental characterizations, the parent enrichment culture is often easier to maintain than the derived pure cultures. Companies

selling bioaugmentation cultures maintain their dechlorinating cultures as consortia. Comparisons of volume-normalized respiration rates of various organohalide

enrichment cultures and pure cultures show that rates vary over more than four

orders of magnitude and, in most cases, organohalide dehalogenation rates by

obligate OHRB are faster in mixed enrichment cultures than in pure cultures (see

Table 14.1 and references therein). Interspecies food webs exist in these enrichments—both among different OHRB populations as well as between non-OHRB

and OHRB. The phylogenetic and metabolic groups that comprise the non-OHRB

populations vary as a function of several factors including electron donor fed, incubation conditions, and type of organohalide substrate as well as the availability of

other types of electron acceptors like sulfate or iron. Though electron donor does

influence community structure, even after enrichment for years on a single electron

donor, organohalide-respiring communities retain diverse fermentation capabilities.

In pristine settings, OHRB are members of a natural organohalide biogeochemical cycle. Sediments and soils harbor natural, albeit small, populations of

OHRB, which is the basis of monitored natural attenuation in contaminated aquifers. At such contaminated field sites, local geochemistry and specific bioremediation enhancement strategies impact the structure of in situ organohalide-respiring

communities. Figure 14.1 presents a schematic of general microbial food web

interactions in organohalide-respiring communities. Included are those interactions common in stable laboratory enrichment cultures (solid lines in Fig. 14.1)



Dhc

Dhc

Dhc

Dhc

Sulfurospirillum

Desulfitobacterium

Dhb (>1 strain)



E



C

P

P

P

P

P

E



KB-1-U of Torontoa



Dhc strain 195

cocultures

Dhc strain 195



Dhc strain 195



Dhc strain FL2



Sulfurospirillum

multivorans

Desulfitobacterium

strain PCE1

ACT-3 (aka MS)a



TCE



TCE



PCE



TCE



PCE



1,1,1-Trichloroethane



PCE



TCE



Dhc (>1 strain)

Geobacter



E



D2a



PCE



Dhc



Dhc, Geobacter



E



DehaloR^2



TCE



Key OHRB

population(s)



Type of

cultureb



Culture namea



Organohalide substrate



Bacteroides,

Desulfovibrio, Clostridium,

Sedimentibacter



None



None



None



None



None



Syntrophomonas,

other Clostridiaceae

Methanospirillum,

Methanosaeta

Acetobacterium,

Sporomusa, Spirochaetes,

Bacteroidetes,

Methanomethylovorans,

Methanomicrobiales,

Methanosaeta, and

Methanosarcina

Desulfovibrio



Acetobacterium,

Clostridium, Spirochaetes



Noted non-OHRB

populations



Table 14.1  Representative respiration rates by various organohalide-respiring cultures normalized per liter of culture



Scholz-Muramatsu

et al. (1995)

Gerritse et al.

(1996)

Grostern and

Edwards (2006a),

Tang et al. (2012)



45

5.6

0.87 (2.4 for

chloroform in

subculture CF)

Methanol,

Ethanol, and

Lactate



(continued)



Maymó-Gatell

et al. (1997)

He et al. (2005)

2.3



Men et al. (2012)

120



Men et al. (2012)



Duhamel et al.

(2002), Duhamel

and Edwards

(2006)



Delgado et al.

(2014), Ziv-El

et al. (2011)

Mansfeldt et al.

(2014), Rowe et al.

(2008)



Reference(s)



3.2



9.2



9.2



82



130



Organohalide

respiration rate

µmole X/L/h

(X = halogen)



Formate



H2



H2



H2



H2



Lactate



Methanol



Butyrate



Lactate and

Methanol



Electron donor



14  Organohalide-Respiring Bacteria as Members of Microbial …

311



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