p273

Landfall of animals

The landfall of animals may have been facilitated by a symbiotic relationship with gut microbes. If cellulases in Metazoa were all from microbial origin, the story may have been simple, but the actual events may be complicated.

There is no doubt about the last common ancestors of Metazoa having had endo-β-1,4-glucanase {and glucosidase):

N. Lo, H. Watanabe, and M. Sugimura, “Evidence for the presence of a cellulase gene in the last common ancestor of bilaterian animals,” 

Proc. Roy. Sc.  270 , S69 (2003)

Positional identity in the introns of cellulase genes from a termite, a sea squirt and an abalone provided compelling evidence that a similar gene was present in the last common ancestor of protostomes and deuterostomes. At least one family of of endogenous cellulases may be more widespread in animals than previously thought. 

H Watanabe, G Tokuda, Cellulolytic Systems in Insects, 

Ann Rev Entomology  55 609 (2009)

is a recent review, and it is clearly stated that the above mentioned cellulase was not due to lateral gene transfer.

However, was the own cellulase enough? The extant termites without ciliate symbionts were regarded using only their own cellulase, but if gut bacteria were removed by antibiotics, their cellulase activity was greatly reduced:

Tokuda et al., “Hidden cellulases in termites: revision of an old hypothesis,” 

Biol. Lett.  3 , 336 (2007). 

75% of all termite species do not harbor the cellulolytic flagellates; the endogenous cellulase secreted from the midgut tissue has been considered a sole source of

cellulases in these termites Antibiotic treatment administered to  Nasutitermes takasagoensis  significantly reduced cellulase activity in the hindgut, suggesting that these cellulases were produced by symbiotic bacteria.

As to the metagenomics of gut flora

Warnecke et al., “Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite,” 

Nature  450 , 560 (2007)

Metagenomic analysis of the bacterial community resident in the hindgut paunch of a wood-feeding ‘higher’  Nasutitermes species (which do not contain cellulose-fermenting protozoa) to show the presence of a large, diverse set of bacterial genes for cellulose and xylan hydrolysis.

Gut symbionts as a source of nitrogen may have also been important:

Hongoh et al., “Genome of an Endosymbiont Coupling N2 Fixation to Cellulolysis Within Protist Cells in Termite Gut,” 

Science  322 , 1108 (2008).

The complete genome sequence of the uncultured Bacteroidales endosymbiont of the cellulolytic protist  Pseudotrichonympha grassii , which accounts for 70% of the bacterial cells in the gut of the termite  Coptotermes formosanus .

∗ Functional annotation of the chromosome (1,114,206 base pairs) unveiled its ability to fix dinitrogen and recycle putative host nitrogen wastes for biosynthesis of diverse amino acids and cofactors, and import glucose and xylose as energy and carbon sources.

∗ Nitrogen fixation and cellulolysis are coupled within the protist’s cells.

Chaffron et al., “Termites in the woodwork,” 

Genome Biol.  8 , 229 is a review: 

Microbes found in the termites’ hindguts possess just the right tools.

To utilize woody parts of plants, lignin must be digested, but it is possible only for limited groups of fungi:

Only a small group of fungi―termed white rot fungi―are able to degrade lignin, and as a consequence, these fungi play an important role in the global carbon cycle. [Birren et al., “Genomics of the fungal kingdom: Insights into eukaryotic biology,” Genome Res.  15 , 1620 (2005)]

Therefore, insects that utilize woody parts must have symbiotic fungi:

Geib et al., “Lignin degradation in wood-feeding insects,” 

Proc Natl Acad Sci  105 , 12932 (2008).

∗ Lignin degradation by two insect species, the Asian longhorned beetle ( Anoplophora glabripennis ) and the Pacific dampwood termite ( Zootermopsis angusticollis ).

∗ In A. glabripennis identified a single species of fungus in the  Fusarium solani/Nectria haematococca species complex. This is a soft-rot fungus that may be contributing to wood degradation.

Incidentally, according to the following paper on the genome of panda:

Li et al., The sequence and de novo assembly of the giant panda genome, 

Nature  463 311 (2010),

the adaptation of pandas to bamboos is mainly due to the specialization of gut bacteria.