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REVIEW ARTICLE
Keywords Abstract
Bacilli, intestinal microbiota, invertebrates,
termites. Soil invertebrates harbour a complex microbial community in their intestinal
system. The total number of microbes in the hindgut of soil invertebrates can
Correspondence reach a titre of 1011 ml)1. The gut microbes play an indispensable role in the
Helmut König, Institut für Mikrobiologie und digestion of food and are of ecological importance in the global carbon cycle.
Weinforschung, Johannes Gutenberg-
The gut microbiota can include a variety of micro-organisms from the three
Universität Mainz, Becherweg 15, D-55099
Mainz, Germany.
domains Bacteria, Archaea and Eucarya. The bacterial groups from the intesti-
E-mail: hkoenig@uni-mainz.de nal systems are mainly affiliated to the proteobacteria, the gram-positive groups
Firmicutes and Actinobacteria, the Bacteroides/Flavobacterium branch and the
2005/1159: received 3 October 2005, revised spirochetes. The Archaea are represented by methanogens. The eukaryotic
25 November 2005 and accepted 25 Novem- groups consist of protozoa, yeasts and fungi. Intestinal bacteria are involved in
ber 2005 the degradation of cellulose, hemicellulose and aromatic compounds as well as
nitrogen fixation. They also contribute to the redox status of the gut. Bacilli
doi:10.1111/j.1365-2672.2006.02914.x
form a significant portion of the intestinal microbial community of soil inver-
tebrates, especially among cellulose degraders. The diversity and function of
bacilli in soil invertebrates will be discussed in this paper.
622
I Stage II Stage III Stage
Hydrolytic Oxidative/fermentative Acetogenic bacteria, methanogenic
Substrate micro-organisms micro-organisms archea, sulfate-reducing bacteria
Journal compilation ª 2006 The Society for Applied Microbiology, Journal of Applied Microbiology 101 (2006) 620–627
ª 2006 The Author
H. König Hindgut microbiota of soil invertebrates
Bacillus brevis* Anacanthotermes ahngerianus (h), Krasil’nikov and Satdykov (1969); Wenzel
Zootermopsis angusticollis (l) et al. (2002)
Bacillus cereus Anacanthotermes ahngerianus (h), Krasil’nikov and Satdykov (1969); Thayer
Nasutitermes nigriceps (h), Neotermes (1976); Schäfer et al. (1996); Kuhnigk and
castaneus (l), Reticulitermes hesperus (l), König (1997)
Reticulitermes santonensis (l)
B. cereus-related isolate* Zootermopsis angusticollis (l) Wenzel et al. (2002)
Bacillus circulans-related isolate* Zootermopsis angusticollis (l) Wenzel et al. (2002)
Bacillus coagulans Mastotermes darwiniensis (l) Schäfer et al. (1996)
Bacillus firmus Reticulitermes santonensis (l) Kuhnigk (1996)
Bacillus licheniformis Reticulitermes santonensis (l) Kuhnigk et al. (1994); Schäfer et al. (1996);
Kuhnigk and König (1997)
Bacillus megaterium* Anacanthotermes ahngerianus (h), Krasil’nikov and Satdykov (1969);
Mastotermes darwiniensis (l), Zootermopsis Mannesmann and Piechowski (1989);
angusticollis (l) Kuhnigk (1996); Wenzel et al. (2002)
Bacillus mycoides Anacanthotermes ahngerianus (h) Krasil’nikov and Satdykov (1969)
Bacillus oleronius Reticulitermes santonensis (l) Kuhnigk et al. (1995)
Bacillus sp. Schedorhinotermes intermedius (l), Eutick et al. (1978); Mannesmann and
Coptotermes acinaciformis (l), Coptotermes Piechowski (1989); Kuhnigk (1996)
formosanus (l), Heterotermes indicola (l)
Bacillus sphaericus Odontotermes distans (h), Odontotermes Kuhnigk (1996); Schäfer et al. (1996);
obesus (h), Reticulitermes santonensis (l), Kuhnigk and König (1997)
Zootermopsis angusticollis (l)
Bacillus subtilis Anacanthotermes ahngerianus (h), Krasil’nikov and Satdykov (1969); Schäfer
Reticulitermes santonensis (l) et al. (1996); Kuhnigk and König (1997)
Paenibacillus macerans Mastotermes darwiniensis (l) Schäfer et al. (1996)
Paenibacillus sp.* Zootermopsis angusticollis (l) Wenzel et al. (2002)
l ¼ lower termite, h ¼ higher termite; * ¼ cellulolytic activity was shown; ¼ hemicellulolytic activity was shown; ¼ capability to degrade aro-
matic compounds was shown.
% of N from
% Sequence Source of Reduction of Reduction Production nitrate or nitrite
Closest relative (accession no.) similarity closest relative nitrate of nitrite of N2 recovered in N2O
were related to Erwinia amylovora, Staphylococcus captitis related to Paracoccus denitrificans, S. maltophilia, and
and Pantoea agglomerans. The ascomycete Acremonium Bacillus weihenstephaniensis were identified (Jensen et al.
charticola was also found. Other isolates could be assigned 2003). Microarthropods like collembola and mites
to the genera Ochrobactrum, Alcaligenes, Comomonas, enhance the destruction of organic material. The gut con-
Pseudomonas and Paracoccus (Hoffmann et al. 1998). By a tents of F. candida also showed fungal mycelia (Tochot
cultivation-independent molecular approach, bacteria et al. 1982) after feeding with hornbeam (Carpinus betu-
lus) leaves. A Bacillus sp. was isolated from faeces with a Bignell (1984) found actinomycete-like filaments
capacity to degrade chitin (Hale 1967). attached to cuticular surfaces of Cylindroiulus sp. The
inner surface of the intestinal walls of the millipedes
Chromatoiulus rossicus and Glomeris connexa is colonized
Isopoda
by bacteria of different morphotypes.
The cosmopolitan isopods live in diverse habitats ranging Yeast cells colonize mainly the hindgut of G. connexa,
from marine environments to dry habitats-like deserts. Leptoiulus polonicus and Megaphyllum projectum. (Byzov
More than one-third of the described isopodan species et al. 1993b).
belong to the terrestrial woodlice (Schamlfuss, 2003). Spe- Ineson and Anderson (1985) found 2Æ8 · 109 CFU g)1
cies like Porcellio scaber and Oniscus asellus are among dry weight in the whole gut of the diplopod Glomeris
the most studied species (Hopkin 1989; Drobne 1997; marginata. The numbers of bacteria isolated from the
Kostanjšek et al. 2005). peritrophic membrane of G. connexa were similar to those
The oniscidean digestive system has been extensively in the gut tissue (c. 107 CFU g)1 dry membrane (Byzov
studied (Hames and Hopkin 1989; Štrus et al. 1995; et al. 1996).
Molnar et al. 1998; Zimmer 2002). The digestive system Most of the bacterial strains isolated from the millipede
of terrestrial isopods consists of a foregut comprising guts and the gut contents belong to the gamma subclass
oesophagus and stomach, a midgut presented mainly by of Proteobacteria and the Actinobacteria. The dominant
tubular midgut glands and a hindgut. An autochtonous bacteria found by many authors inhabiting the guts
flora has been demonstrated (Kostanjšek et al., 2002). belong to facultative anaerobic bacteria of the family
Three bacillus isolates have been characterized. Two Enterobacteriaceae with the genera Klebsiella, Enterobacter,
strains of Bacillus cereus and an other Bacillus strain were Plesiomonas, Salmonella, Erwinia and Escherichia, and
isolated from the gut of P. scaber (Kostanjšek et al. 2005). Vibrio from the Vibrionaceae (Byzov 2005). Free metha-
nogenic prokaryotes and ciliates (Nyctotherus type) with
intracellular endosymbiotic methanogens have been detec-
Millipedes
ted microscopically by their characteristic autofluores-
Soil millipedes (Diplopoda) possess a specific gut cence in the hindguts of the tropical diplopods Chicobolus
microbiota that differs from microbial communities in sp., Orthoporus sp., Rhapidostreptus virgator and two
soil and leaf litter. A diverse microbiota has been found unidentified species (Hackstein and Stumm, 1994).
by dilution plating from the gut and includes gamma Most of yeast strains isolated from the millipede guts
proteobacteria, actinobacteria and yeasts (Byzov 2005). and the gut contents are ascomycetes. In Pachyiulus
Microscopic studies also revealed a variety of morpho- flavipes, the predominating species were Debaryomyces
types of bacteria and yeasts attached to the gut walls hansenii, Torulaspora delbrueckii, Zygowilliopsis californicus
(Byzov 2005). (¼Williopsis californica) and Pichia membranaefaciens
The foregut of millipedes is poorly populated by micro- (Byzov et al. 1993a). Several isolates assigned to the genus
organisms. The midgut represents the absorptive surface Bacillus have been isolated (Table 4).
and continuously secretes the semipermeable peritrophic
membrane. The cuticle-lined hindgut is strongly developed
Conclusions
and bears both flat cuticular surfaces and ornaments such
as spines of various shapes, which provide sites for micro- Contrary to previous speculation that invertebrates
bial colonization. (Crawford et al. 1983). such as earthworms and springtails possessed no auto-
chthonous microbiotas, convincing evidence now exists of Byzov, B.A., Thanh, V.N. and Bab’eva, I.P. (1993b) Interrela-
distinctive intestinal communities, which can contribute tionships between yeasts and soil diplopods. Soil Biol Bio-
to the degradation of recalcitrant biological materials such chem 25, 1119–1126.
as chitin and lignocellulose. Bacilli, in particular, can take Byzov, B.A., Chernjakovskaya, T.F., Zenova, G.M. and Dobro-
part in the early and intermediate steps of polymer degra- volskaya, T.G. (1996) Bacterial communities associated
dation (Table 1). They posses cellulolytic and hemi- with soil diplopods. Pedobiologia 40, 67–79.
cellulolytic activities and some can also degrade aromatic Chen, B., Snider, R.J. and Snider, R.M. (1995) Food preference
compounds, if the partial pressure of oxygen is sufficient and effects of food type on the life history of some soil
Collembola. Pedobiol 39, 496–505.
(Kuhnigk et al. 1994, 1995; Kuhnigk 1996; Kuhnigk and
Chen, B., Snider, R.J. and Snider, R.M. (1996) Food consump-
König 1997).
tion by collembola from northern Michigan deciduous
In contrast to the rumen, where strictly anaerobic
forest. Pedobiol 40, 149–161.
cellulolytic bacteria belonging to the genera Ruminococcus,
Coleman, D.C. and Crossley, D.A. Jr. (1996) Fundamentals of
Butyrivibrio and Bacteroides are present, the cellulolytic
Soil Ecology. San Diego: Academic Press.
bacteria in the termite gut are facultatively anaerobic or Crawford, C.S., Minion, G.P. and Bayers, M.D. (1983)
microaerophilic bacteria. Species of the genera Bacillus are Intima morphology, bacterial morphotypes, and effects
predominant with titres of up to 107 ml)1 gut contents of annual molt on microflora in the hindgut of the
(Wenzel et al. 2002), and bacilli play a major role in the desert millipede Orthoporus ornatus (Girard) (Diplopoda:
guts of invertebrates in the first and second step (Table 1) Spirostreptidae). Int J Insect Morphol Embryol 12,
of the degradation of polymeric material under oxygen 301–312.
limitation. Drake, H.L., Schramm, A. and Horn, M. (2005) Earthworm
gut microbial biomes: their importance to soil microor-
ganisms, denitrification, and the terrestrial production of
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