Natural paradigms of plant cell wall degradation

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Natural processes of recycling carbon from plant cell walls are slow but very efficient, generally involving microbial communities and their secreted enzymes. Efficient combinations of microbial communities and enzymes act in a sequential and synergistic manner to degrade plant cell walls. Recent understanding of plant cell wall ultra-structure, as well as the carbon metabolism, ATP production, and ecology of participating microbial communities, and the biochemical properties of their cellulolytic enzymes have led to new perspectives on saccharification of biomass. Microbial communities are dynamic functions of the chemical and structural compositions of plant cell wall components. The primitive ‘multicellularity’ exhibited by certain cellulolytic microorganisms may play a role in facilitating cell–cell communication and cell–plant cell wall–substrate interaction.

Introduction

Plants capture energy from sunlight, converting carbon dioxide and water into carbohydrates through the process of photosynthesis, thereby providing, directly or indirectly, most of the energy utilized by life on Earth. Through photosynthesis, tremendous amounts of energy are sequestered in the chemically and structurally complex polysaccharide networks that make up plant cell walls—the primary component of plant biomass. Enzymatic decay of biomass by microbial communities in nature releases carbon back into the global carbon cycle. Cellulolytic microbial communities are ubiquitous in nature and most are associated with plant residues in soils, swamps, sewage sludge, aquatic ecosystems (including rivers, lakes, seawater sediments, springs, etc.), and compost heaps. They also exist in the guts of wood-eating worms, termites, and vertebrate herbivores. Recent reviews and research articles have addressed microbes and enzymes of the rumen [1], termites [2], and aquatic ecosystems [3, 4]. This review pertains to microorganisms and enzyme systems occurring in soils, wood/leaf-litters, and composts.

Lignocellulosic biomass can be converted to simple sugars and fermented to liquid fuels through chemical and biological processes; currently consisting of sequential steps of thermo-chemical pretreatment, enzymatic saccharification, and fermentation. However, this process stream is inefficient and requires expensive capital equipment investments. The major bottleneck in conversion technology is the recalcitrance of plant cell walls to efficient deconstruction to simple sugars. This can be mitigated by increasing sugar yield during thermo-chemical pretreatment, by improving enzyme performance and/or reducing the production cost of enzymes used for saccharification, and by developing ethanologenic strains that efficiently ferment mixtures of C-5 and C-6 sugars.

New concepts have been proposed to enable the overall goal of cost-reduction, including genetically modifying the cell wall composition of energy crops in order to make their conversion ‘easier’ [5, 6, 7], and combining the processes of glycoside hydrolase enzyme production, saccharification and fermentation (consolidated bioprocessing, or CBP) [8•, 9].

In the current report, we review recent understanding of the diversity of plant biomass, associated microbial communities and enzymes, and the interactions and correlations between them. Perspectives and suggestions are given in the context of improving microbial efficiency in carbon utilization and ATP production, and utilizing both endophytic and saprotrophic microorganisms with the overall goal of producing cost-effective biofuels from biomass.

Section snippets

Plant cell walls are complex and dynamic: recalcitrance to deconstruction

Cell wall structure and composition vary between different plant species, different tissues and cells, primary and secondary walls in the same cell, and even different layers within the same cell wall. The chemical and structural complexity of plant cell walls that enables their diverse biological functions, including mechanical support, protection against pathogens, and regulation and transport of material (i.e. water and solutes) at the cellular and organismal levels, are also the root causes

Natural cellulolytic paradigms: succession, diversity, and correlative interaction

Figure 1 compares the bacterial and fungal mass contributions in various ecosystems, such as the terrestrial systems (soils, and wood/leaf-litters), composts (a semi-natural system) and rumen (a highly specialized and finely controlled anaerobic system) [1, 3, 8•, 21, 22, 23, 24, 25, 26, 27].

Profound differences are noted between aerobic and anaerobic microorganisms regarding their cellulase systems, ATP production, cell mass yield, and end products of cellulolytic biomass degradation, as

A missing part of the picture: microorganisms having both endophytic and saprotrophic lifestyles

So far we have discussed saprophytic microbial communities, that is, those that primarily colonize and degrade dead plant biomass. However, another important microbial community often overlooked is that of the endophytes living on the surface of or inside the living plant body. The density of endophytes inside plants can be quite high, with up to 1 × 105 cfu (colony forming units) per gram plant tissue [54], and the number of colonizing endophytic fungal species can also be substantial, being

Perspectives and directions for future research

It seems that nature has not evolved ‘super’ organisms or enzymes that we can use today for rapidly saccharifying plant cell walls. We may have to accept the limitation that although we may be able to improve the efficiency of biomass conversion, the rate will still be slow by process-engineering standards. Given this, what can we learn from natural paradigms and how can we improve the conversion efficiency for biofuel production? Besides traditional approaches to improving enzyme performance,

Conclusion

The plant cell wall–microbe–enzyme relationship is the foundation of plant biomass degradation in natural environments. Investigations of natural systems have demonstrated that the complexities of each of these three partners are correlated with the recalcitrant features of plant cell wall materials. The overall energy level of the system is dependent on the available carbon source. On the basis of current understanding of natural paradigms, we propose that multi-microorganism bioprocessing

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgement

This work was supported by the Laboratory Directed Research and Development (LDRD) Program at the National Renewable Energy Laboratory.

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