Journal of Applied Microbiology ISSN 1364-5072

REVIEW ARTICLE

Bacillus species in the intestine of termites and other soil

invertebrates
H. König
Institut für Mikrobiologie und Weinforschung, Johannes Gutenberg-Universität Mainz, Mainz, Germany

Keywords
Bacilli, intestinal microbiota, invertebrates,
termites.
Correspondence
Helmut König, Institut für Mikrobiologie und
Weinforschung, Johannes Gutenberg-
Universität Mainz, Becherweg 15, D-55099
Mainz, Germany.
E-mail: hkoenig@uni-mainz.de
2005/1159: received 3 October 2005, revised
25 November 2005 and accepted 25 Novem-
ber 2005
doi:10.1111/j.1365-2672.2006.02914.x
Abstract
Soil invertebrates harbour a complex microbial community in their intestinal
system. The total number of microbes in the hindgut of soil invertebrates can
reach a titre of 1011 ml)1. The gut microbes play an indispensable role in the
digestion of food and are of ecological importance in the global carbon cycle.
The gut microbiota can include a variety of micro-organisms from the three
domains Bacteria, Archaea and Eucarya. The bacterial groups from the intesti-
nal systems are mainly affiliated to the proteobacteria, the gram-positive groups
Firmicutes and Actinobacteria, the Bacteroides/Flavobacterium branch and the
spirochetes. The Archaea are represented by methanogens. The eukaryotic
groups consist of protozoa, yeasts and fungi. Intestinal bacteria are involved in
the degradation of cellulose, hemicellulose and aromatic compounds as well as
nitrogen fixation. They also contribute to the redox status of the gut. Bacilli
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.

rDNA sequence analysis), it was possible to get a rough

Introduction
Soil is an important natural habitat for a large number of
prokaryotes as well as lower and higher animals (Coleman
and Crossley 1996; König and Varma 2005). Microbes
and especially many invertebrates play a major role in the
degradation of organic material in the soil. Although
invertebrates such as termites are able to degrade natural
polymers, e.g. lignocellulose, with the assistance of their
mutualistic microbiota, the contribution of such gut
microbes to natural decomposition processes has been
neglected while the attention of soil biologists focused
mainly on free-living or particle-bound micro-organisms.
The role of intestinal microbes in the recycling of organic
matter occurring in gut systems of soil animals has often
been disregarded.
The primary decomposers of organic soil litter are the
lumbricides, the diplopods, the isopods, and the dipteran
larvae as well as termites in subtropical and tropical
regions. Only a small portion of the intestinal microbes
of soil invertebrates has been screened axenically. How-
ever, with the aid of molecular methods (e.g. total 16S
estimate of the total population in some gut systems of
soil invertebrates. Since the pioneering investigations of
Buchner (Buchner 1953) about the microbes of the intes-
tine of invertebrates, the knowledge of the identity and
physiology of intestinal microbial species has been scarce
for a long time. In the last years, the intestinal microbial
community (microbiota) of some soil invertebrates such
as collembola, earthworms, isopods, millipedes and ter-
mites has been studied in more detail. In all investigated
soil invertebrates, bacilli are part of the microbiota. This
article will only deal with this group.
Termites
Termites thrive between the 47 latitude north and 47
latitude south, which accounts for 68% of the earth’s sur-
face. Their main area of distribution is of course in trop-
ical and subtropical regions (Krishna 1970). The total
population is estimated to be 2Æ4 · 1017 individual ter-
mites (Zimmerman et al. 1982). Termites (Isoptera) and
ants (Formicidae) represent 80% of the individual insects

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620 Journal compilation ª 2006 The Society for Applied Microbiology, Journal of Applied Microbiology 101 (2006) 620–627
H. König
P3a
P3b
P5
P1
MT
F P4
H
M genera Ruminococcus, Butyrivibrio and Bacteroides are pre-
Figure 1 The isolated gut of the Australian termite Mastotermes dar-
winiensis. Bar ¼ 5 mm. Intestine. F ¼ forgut with salivary glands,
esophagus, crop and gizzard; M ¼ Midgut; MT ¼ malpighian tubules;
H ¼ hindgut; P1 ¼ proctodeal segment of the hindgut followed by
the enteric valve; P3a ¼ thin-walled part of the paunch, P3b ¼ thick
walled part of the paunch; P4 colon; P5 ¼ rectum (modified from
König et al. 2005).
and 30% of the total animal biomass near Manaus in
Brazil (Fittkau and Klinge 1973). The digestive system of
termites consists of the foregut with the crop and the giz-
zard, the midgut and the hindgut (Fig. 1; Noirot and
Noirot-Timotheé 1969; Noirot 1995). Even if their gut is
very small, because of the high number of individuals,
they play a major role in the degradation of organic
material. Because of their intestinal flora, termites are
among the most important wood- and litter-feeding
insects (Wood and Sands 1978).
The termite gut can be described as an anaerobic gradi-
ent system, which is constantly supplied with oxygen via
the epithelium. Examinations using microelectrodes have
shown a pronounced spatial differentiation of termite
hindguts with respect to pH (Noirot, 1995; Noirot and
Noirot-Timotheé 1969; Brune and Kühl 1996) and axial
or radial gradients of oxygen or hydrogen.
In recent years, a larger proportion of intestinal org-
anisms have been characterized and their phylogenetic
position determined. Although several hundred microbial
clones/strains have been identified by 16S rRNA sequence
analysis or were obtained in pure culture from the termite
gut, many microbial species remain uncultured and there-
fore uninvestigated (Table 1; Breznak and Brune 1994;
Brune 1998; König et al. 2002; Ohkuma 2003; König et al.
2005; Ohkuma et al. 2005).
The paunch of termites is about 108 times smaller than
a rumen resulting in a 500 times larger oxygen influx per
unit volume (Brune 1998). Because of the small size, the
transit time of the food through the intestinal tract is
only about 24 h (Breznak 1984). These facts have signifi-
cant influences on the composition of the microbial flora.
ª 2006 The Author
Journal compilation ª 2006 The Society for Applied Microbiology, Journal of Applied Microbiology 101 (2006) 620–627
Hindgut microbiota of soil invertebrates
In the hindgut of termites, both strictly aerobic and
microaerophilic bacteria are readily isolated (König et al.
2002).
Several Bacillus and Paenibacillus species have been
detected in the termite gut (Table 2; Kuhnigk et al. 1994,
1995; Kuhnigk 1996; Kuhnigk and König 1997). They
may play a role in the digestion of polysaccharides and
aromatic compounds. In contrast to the rumen, where
strictly anaerobic cellulolytic bacteria belonging to the
sent, the cellulolytic bacteria in the termite gut are facul-
tatively anaerobic or microaerophilic bacteria. Species of
the genera Bacillus are predominant with titres of up to
107 ml)1 gut contents (Wenzel et al. 2002).
Earthworms
Earthworms contribute significantly to the recycling of
organic matter in soil (Edwards and Bohlen 1996). Their
gut microbiota have only been partially identified. Most
isolates were affiliated with the gamma subclass of the
class Proteobacteria or with the gram-positive bacteria
with low DNA G + C contents. Bacilli and paenibacilli
have been identified (Table 3). Gut-associated micro-
organisms are responsible for the capacity of earthworms
to emit nitrous oxide (N2O) (Ihssen et al. 2003; Drake
et al. 2005). The abundance of microbes which use nitrate
as a terminal electron acceptor were c. 2 orders of magni-
tude higher in the earthworm gut than in the soil.
Gut passage also enhances the germination of Bacillus
spores (Fischer et al. 1997) and increases the detectability
of bacteria by fluorescence in situ hybridization (FISH)
(Fischer et al. 1995; Schönholzer et al. 2002).
Springtails
The about 7Æ500 collembola species (springtails) are
between 0Æ2 mm and 1 cm in size. Collembola are among
the most abundant arthropods on earth (Hopkin 1997;
Tebbe et al. 2005). With an age of about 400 · 106 years,
they are probably the oldest hexapods. Their habitats are
mainly soil or litter.
Collembola ingest live or dead organic material from
plants; or prey on animals such as nematodes and micro-
organisms such as fungi (Chen et al. 1995, 1996; Thimm
and Larink 1995). The gut has a volume of only some
nanolitres (Thimm et al. 1998). In Folsomia candida,
4 · 1011 CFU g)1 faeces were determined (Borkott and
Insam 1990a,b).
These included the two chitin-degrading bacteria
Stenotrophomonas maltophilia and Curtobacterium sp.
From the gut of F. candida, 45 different bacterial pure
cultures were established (Thimm et al. 1998). The strains
621
 Table 1 Intestinal isolates involved in the different stages of lignocellulose degradation in the termite gut

622
I Stage II Stage III Stage
Hydrolytic Oxidative/fermentative Acetogenic bacteria, methanogenic
Substrate micro-organisms micro-organisms archea, sulfate-reducing bacteria

Wood mechanical Cellulose Cellulase b-Glucosidase

degradation to (34–62%) Flagellates: Trichomitopsis
micrometre particles termopsidis, Trichonympha sphaerica
by termites Bacteria: Alcaligenes,
Azospirillum, Bacillus, Brevibacillus,
Cellulomonas-related spp.,
Clavibacter, Clostridium,
Corynebacterium, Klebsiella,
Actinobacteria, Arthrobacter, Food source of termites:
Aureobacterium, Bacillus, Citrobacter, Acetate, propionate,
Enterobacter, Enterococcus, Klebsiella, butyrate, microbial cells
Lactococcus, Nocardia, Ochrobactrum,
Pseudomonas, Rhizobia, Rhodococcus,
Hindgut microbiota of soil invertebrates

Kocuria, Paenibacillus, Microbacterium, Serratia, Streptomyces

Micromonospora, Nocardioforme,
Rhizobia,
Ochrobactrum, Paenibacillus,
Sphingomonas, Spirosoma-
related spp., Streptomyces
Yeasts: (Cryptococcus, Filobasidium) Yeasts
Hemicellulose 1Æ4-b-Xylanase b-D-Galactosidase 2H2 + O2 H2O Excreted end products:
(14–32%) 1Æ3-b-Galactanase a-L-Arabinosidase Lactate  Acetate + CO2 CO2, H2, CH4
Actinobacteria, Acinetobacter, b-L-xylosidase Desulfovibrio Microbial cells
Bacillus, Flavobacterium- Actinobacteria, Acinetobacter, 4H2 + 2CO2  Acetate + 2 H2O
related spp., Ochrobactrum, Arthrobacter, Aureobacterium, Acetonema, Clostridium,
Paenibacillus, Pseudomonas, Bacillus, Burkholderia, Citrobacter, Sporomusa, Spirochetes
Streptomyces Cellulomonas, Enterobacter, 4 H2 + CO2  CH4 + 2 H2O
Escherichia, Klebsiella, Nocardia, Methanobrevibacter
Ochrobactrum, Pseudomonas,
Paenibacillus, Rhizobium, Serra-tia,
Staphylococcus, Streptomyces
Yeasts: (Candida, Yeasts
Debaryomyces,
Pichia, Sporothrix)
Aromatic Acinetobacter, Arthrobacter, Alcaligenes,
compounds Aureobacterium, Bacillus, Burkholderia,
(5%) Citrobacter, Comamonas,
Enterobacter, Klebsiella, Listeria,
Nocardia, Ochrobactrum,
Pseudomonas, Rhizobia, Serratia,
Streptomyces
Lignin Streptomyces Excreted: modified lignin
(18–39%)
N2-fixation Enterobacter, Desulfovibrio, Rhizobia,
Klebsiella, Spirochetes, Citrobacter

From König et al. (2005).

H. König

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

Table 2 Bacilli from the termite gut

Species Termite Reference

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.

Table 3 Bacilli from the earthworm Aporrectodea caliginosa

% 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

Bacillus mycoides 100 Soil + 0 ) <0Æ5

B. mycoides 100 Soil + 0 ) 7
Paenibacillus sp. strain P51-3 100 Vegetable purees + + ) 6
Paenibacillus sp. strain P51-3 97Æ8 Vegetable purees + + ) 3
Paenibacillus sp. strain P51-3 99 Vegetable purees + 0 ) 3
Paenibacillus sp. strain 61724 99Æ5 Soil + + ) 11
Paenibacillus burgondia B2 99Æ1 Mycorhizosphere + + ) 8
Paenibacillus borealis KK19 95 Soil ) + ) 10
Paenibacillus amylolyticus NRRL B-290T 100 Soil ) + ) <0Æ5

From Ihssen et al. (2003).

were related to Erwinia amylovora, Staphylococcus captitis
and Pantoea agglomerans. The ascomycete Acremonium
charticola was also found. Other isolates could be assigned
to the genera Ochrobactrum, Alcaligenes, Comomonas,
Pseudomonas and Paracoccus (Hoffmann et al. 1998). By a
cultivation-independent molecular approach, bacteria
related to Paracoccus denitrificans, S. maltophilia, and
Bacillus weihenstephaniensis were identified (Jensen et al.
2003). Microarthropods like collembola and mites
enhance the destruction of organic material. The gut con-
tents of F. candida also showed fungal mycelia (Tochot
et al. 1982) after feeding with hornbeam (Carpinus betu-

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Journal compilation ª 2006 The Society for Applied Microbiology, Journal of Applied Microbiology 101 (2006) 620–627 623
Hindgut microbiota of soil invertebrates
lus) leaves. A Bacillus sp. was isolated from faeces with a
capacity to degrade chitin (Hale 1967).
Isopoda
The cosmopolitan isopods live in diverse habitats ranging
from marine environments to dry habitats-like deserts.
More than one-third of the described isopodan species
belong to the terrestrial woodlice (Schamlfuss, 2003). Spe-
cies like Porcellio scaber and Oniscus asellus are among
the most studied species (Hopkin 1989; Drobne 1997;
Kostanjšek et al. 2005).
The oniscidean digestive system has been extensively
studied (Hames and Hopkin 1989; Štrus et al. 1995;
Molnar et al. 1998; Zimmer 2002). The digestive system
of terrestrial isopods consists of a foregut comprising
oesophagus and stomach, a midgut presented mainly by
tubular midgut glands and a hindgut. An autochtonous
flora has been demonstrated (Kostanjšek et al., 2002).
Three bacillus isolates have been characterized. Two
strains of Bacillus cereus and an other Bacillus strain were
isolated from the gut of P. scaber (Kostanjšek et al. 2005).
Millipedes
Soil millipedes (Diplopoda) possess a specific gut
microbiota that differs from microbial communities in
soil and leaf litter. A diverse microbiota has been found
by dilution plating from the gut and includes gamma
proteobacteria, actinobacteria and yeasts (Byzov 2005).
Microscopic studies also revealed a variety of morpho-
types of bacteria and yeasts attached to the gut walls
(Byzov 2005).
The foregut of millipedes is poorly populated by micro-
organisms. The midgut represents the absorptive surface
and continuously secretes the semipermeable peritrophic
membrane. The cuticle-lined hindgut is strongly developed
and bears both flat cuticular surfaces and ornaments such
as spines of various shapes, which provide sites for micro-
bial colonization. (Crawford et al. 1983).
Group/genus/species Host
Bacillus sp. Schizophyllum sabulosum var. rubripes
Bacillus spp. Chromatoiulus projectus, Cylindroiulus boleti
Bacillus spp. Pachyiulus flavipes
Bacillus spp. P. flavipes
Bacillus megaterium, Glomeris connexa, Chromatoiulus rossicus
B. cereus, B. licheniformis
Bacillus sp. Ommatoiulus sabulosus
Bacillus brevis Glomeris sp.
From Byzov (2005).
624 Journal compilation ª 2006 The Society for Applied Microbiology, Journal of Applied Microbiology 101 (2006) 620–627
H. König
Bignell (1984) found actinomycete-like filaments
attached to cuticular surfaces of Cylindroiulus sp. The
inner surface of the intestinal walls of the millipedes
Chromatoiulus rossicus and Glomeris connexa is colonized
by bacteria of different morphotypes.
Yeast cells colonize mainly the hindgut of G. connexa,
Leptoiulus polonicus and Megaphyllum projectum. (Byzov
et al. 1993b).
Ineson and Anderson (1985) found 2Æ8 · 109 CFU g)1
dry weight in the whole gut of the diplopod Glomeris
marginata. The numbers of bacteria isolated from the
peritrophic membrane of G. connexa were similar to those
in the gut tissue (c. 107 CFU g)1 dry membrane (Byzov
et al. 1996).
Most of the bacterial strains isolated from the millipede
guts and the gut contents belong to the gamma subclass
of Proteobacteria and the Actinobacteria. The dominant
bacteria found by many authors inhabiting the guts
belong to facultative anaerobic bacteria of the family
Enterobacteriaceae with the genera Klebsiella, Enterobacter,
Plesiomonas, Salmonella, Erwinia and Escherichia, and
Vibrio from the Vibrionaceae (Byzov 2005). Free metha-
nogenic prokaryotes and ciliates (Nyctotherus type) with
intracellular endosymbiotic methanogens have been detec-
ted microscopically by their characteristic autofluores-
cence in the hindguts of the tropical diplopods Chicobolus
sp., Orthoporus sp., Rhapidostreptus virgator and two
unidentified species (Hackstein and Stumm, 1994).
Most of yeast strains isolated from the millipede guts
and the gut contents are ascomycetes. In Pachyiulus
flavipes, the predominating species were Debaryomyces
hansenii, Torulaspora delbrueckii, Zygowilliopsis californicus
(¼Williopsis californica) and Pichia membranaefaciens
(Byzov et al. 1993a). Several isolates assigned to the genus
Bacillus have been isolated (Table 4).
Conclusions
Contrary to previous speculation that invertebrates
such as earthworms and springtails possessed no auto-
Table 4 Bacilli isolated from or detected in
Source the millipede guts and fresh faeces
Gut content
Gut content
Intestinal walls
Gut content
Gut content
Gut content
Hindgut
ª 2006 The Author
H. König
chthonous microbiotas, convincing evidence now exists of
distinctive intestinal communities, which can contribute
to the degradation of recalcitrant biological materials such
as chitin and lignocellulose. Bacilli, in particular, can take
part in the early and intermediate steps of polymer degra-
dation (Table 1). They posses cellulolytic and hemi-
cellulolytic activities and some can also degrade aromatic
compounds, if the partial pressure of oxygen is sufficient
(Kuhnigk et al. 1994, 1995; Kuhnigk 1996; Kuhnigk and
König 1997).
In contrast to the rumen, where strictly anaerobic
cellulolytic bacteria belonging to the genera Ruminococcus,
Butyrivibrio and Bacteroides are present, the cellulolytic
bacteria in the termite gut are facultatively anaerobic or
microaerophilic bacteria. Species of the genera Bacillus are
predominant with titres of up to 107 ml)1 gut contents
(Wenzel et al. 2002), and bacilli play a major role in the
guts of invertebrates in the first and second step (Table 1)
of the degradation of polymeric material under oxygen
limitation.
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